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Article

Foliar Spraying of Mannose Alleviates Cadmium Stress by Changing the Subcellular Distribution and Chemical Forms of Cadmium in Wheat Root

by
Xiang Zheng
,
Xue Cheng
,
Ni Pan
,
Wei Huang
,
Liang Shi
and
Wei Lu
*
College of Life Sciences, Nanjing Agricultural University, Nanjing 210095, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(10), 2273; https://doi.org/10.3390/agronomy12102273
Submission received: 1 September 2022 / Revised: 18 September 2022 / Accepted: 20 September 2022 / Published: 22 September 2022
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Abstract

:
Cadmium (Cd)-contaminated soil has been receiving increasing attention worldwide due to the great harm it causes via food-chain enrichment through crops such as wheat. However, there is little research regarding the effects of mannose (MAN) on plants in response to Cd stress. Hence, hydroponic and potted soil experiments were conducted to investigate the mitigation effects of MAN on wheat under Cd stress and the possible mechanism. Compared with Cd treatment alone, foliar spraying of 160 μM MAN significantly reduced the Cd accumulation in shoots and increased the Cd retention in roots. The content of hemicellulose was increased by MAN treatment, and the proportion of Cd retained by hemicellulose in the cell wall of roots was increased. Furthermore, 160 μM MAN significantly reduced the water-extracted and ethanol-extracted Cd in roots, which are easily transported to shoots. In potted soil experiments using Cd-contaminated soil, MAN reduced the Cd content in wheat grain by 26.3%, compared with the control. These findings indicate that foliar spraying of 160 μM MAN resulted in less Cd being transported from roots to shoots by increasing the Cd retention in the cell wall and changing the Cd chemical forms in roots, which promoted wheat growth and reduced the Cd concentration in wheat grain.

1. Introduction

During periods of rapid industrialization, heavy metals had been widely released into soil, air, and water through human activities such as mineral mining, wastewater irrigation, burning fossil fuels, atmospheric deposition, and the use of fertilizers, pesticides, and paints [1,2]. However, heavy metals are difficult to biodegrade, and their accumulation in the environment poses a serious threat to human health by reducing arable land suitable for farming, reducing food quality, polluting water sources, and damaging ecosystems [3,4]. Among the heavy metals, cadmium (Cd) is deemed a highly toxic pollutant to plants and humans. Cd is easily absorbed by plant roots and enter the edible parts because Cd compounds are relatively more dissolvable and mobile than many other heavy metals [5,6]. Once Cd enters the human body through the food chain, it will cause irreversible damage to multiple organs, especially the kidneys [3,7]. Numerous adverse effects of Cd on the morphology, physiology, biochemistry, metabolism, and ultrastructure in plants have been reported, such as leaf chlorosis and necrosis, browning of roots, growth inhibition, nutritional disorders, restriction of photosynthesis, enzymatic activity inhibition, and basal metabolic disorder [8,9,10]. In addition, Cd toxicity can cause damage to cell membranes, organelles, and biomolecules by stimulating the production of reactive oxygen species (ROS), mainly composed of free hydroxyl ions (OH−) and super-oxide radicals (O2−) [11,12]. Among cereal crops, wheat (Triticum aestivum L.) is the second-most edible staple worldwide, the demand of which is increasing at a fast rate as the world’s population grows [13,14]. Compared with other crops, wheat has a relatively higher Cd transport capacity and Cd tolerance, which may raise Cd accumulation in grain [15]. The absorption of Cd by wheat mainly depends on wheat cultivars, soil contamination degree, and soil type, while the absorption of Cd by grain depends on the root-to-shoot and shoot-to-grain transfer via the xylem–phloem loadings [16].
Various mitigation measures have been used for the alleviation of Cd toxicity to wheat. These measures mainly include the application of using inorganic amendments, such as silicon compounds, phosphorus compounds, and selenium compounds [17]; exogenous application of plant growth regulators, such as gibberellic acid (GA), abscisic acid (ABA), salicylic acid (SA), and jasmonic acid (JA) [18]; adding organic amendments, such as activated carbon [19]; selecting low-Cd-accumulating wheat cultivars [15]; adopting agricultural measures such as intercropping and crop rotation [20]; the application of exogenous microorganisms [21]; and pretreating seeds by microwave or laser [22,23]. However, the effects of mannose by foliar spraying on wheat under Cd stress have not been reported.
Mannose (MAN) is easily absorbed by plants, and previous studies have found that MAN may act on the antioxidant systems of plants [24,25]. It is generally believed that the main site where plants accumulate heavy metals is the cell wall, which is the first barrier for Cd entering into the cells. The cation exchange sites of the cellulose, hemicellulose, lignin, pectin, and other materials that make up the cell wall are rich in active moieties such as carboxyl, hydroxyl, and aldehyde groups [26]. When Cd penetrates the cell wall, it can bind these groups and form a precipitation, which prevent a large amount of Cd from entering the protoplasm and ultimately alleviating the toxicity [27]. Hemicellulose is a heterogeneous polymer composed of several different types of monosaccharides. Hemicellulose is a heterogeneous polymer composed of several different types of monosaccharides, including 5-carbon sugars (such as xylose and arabinose) and 6-carbon sugars (such as MAN and galactose) [28].
In the present study, MAN was applied by foliar spraying on wheat under Cd stress to investigate (1) whether foliar spraying of MAN alleviates the inhibition of growth indicators and photosynthetic capacity induced by Cd stress; (2) the optimal concentration of MAN treatment and its possible mechanisms for its effects on the subcellular distribution and chemical forms of Cd in wheat roots; and (3) whether foliar application of MAN could significantly reduce the Cd content in mature wheat grain.

2. Materials and Methods

2.1. Plant Material, Hydroponic Culture, and Soil Properties

Wheat seeds (cv. sukemai-1) were obtained from Jiangsu Academy of Agricultural Science (Jiangsu Province, China). Briefly, the seeds were vernalized at 20 °C for 1 day and germinated on a nylon net that floated within the deionized water. After one-week, uniform seedlings were transferred to nutrient solution containing 0 (control) or 20 μM CdCl2, and the pH was adjusted to 6.0. Among all Cd stress treatment concentrations, the growth indicators of wheat seedlings under the 20 μM Cd treatment were significantly reduced to about half of the control (Table S1). Therefore, we selected the 20 μM Cd treatment concentration for further study. The wheat seedlings were incubated in a growth chamber (RHQ-350, Jinghong, Shanghai, China), with daytime conditions set at 16 h, 8000 lux, 60% humidity, and 25 °C, while the nighttime parameters were set at 8 h, 0 lux, 80% humidity, and 18 °C. Each treatment had four duplicate pot replicates, with eight wheat seedlings in each pot. After the samples were collected, the eight wheat seedlings were randomly selected for follow-up experiments.
The soil for the potted soil experiments was taken from the surface soil layer (0–20 cm) of an agricultural field near the Yinmao lead–zinc mine (N 32°09′11.39″, E 118°57′15.18″). The potted soil experiments were conducted from October 2018 to June 2019 in the test field located at the Nanjing Agricultural University Pailou experimental base (N 32°01′13.19″, E 118°51′6.14″). The study area is within the north subtropical humid climate and has an annual average temperature of 15.7 °C, annual sunshine average of 2014.4 h, annual average rainfall of 117 days and 1106.5 mm, and a frost-free period of 237 days. The basic chemical properties of the soil at the onset of the experiment are listed in Table 1.

2.2. Experimental Design

Firstly, we sought which MAN concentration is the best to mitigate Cd-induced damage by these indicators: the growth of wheat and the reduction in Cd accumulation. The plant leaves were sprayed every morning with a 15 mL volume of 0, 40, 80, 160, 320, and 640 µM D-mannose. The MAN (>99.9%) was bought from Sigma (Shanghai, China). Seedlings without Cd or MAN treatment was used as the control. Referring to the experimental design of Upadhyay and Chauhan [29], the treatments were designated as (1) deionized water (Con); (2) Cd + deionized water (Cd); (3) Cd + 40 μM MAN; (4) Cd + 80 μM MAN; (5) Cd + 160 μM MAN; (6) Cd + 320 μM MAN; and (7) Cd + 640 μM MAN. Secondly, in order to study how MAN reduces the Cd concentration in the above-ground parts, we chose an optimum MAN concentration (160 μM). The four treatments were control (Con), Cd, Con + MAN, and Cd + MAN, based on our previous experiment results. The Hoagland nutrient solution was composed of 6 mM KNO3, 5 mM CaCl2, 1 mM NaH2PO4, 2 mM MgSO4, 0.025 mM H3BO3, 2 μM MnCl2, 1 μM ZnSO4, 0.1 μM (NH4)6Na7MoO24, 0.25 μM CuSO4, and 10 μM Fe-EDTA. The nutrient solutions were renewed every three days. After two weeks of treatment, wheat seedlings were harvested for further analysis.
The potted soil experiments were selected to study the effects of the foliar spraying of MAN on Cd transport in wheat. Each pot was filled with 8 kg soil. Twenty seeds of the wheat were sown into each pot and later thinned to seven plants per pot on the completion of the third leaf development. For each pot, 5 g of compound fertilizer and 3 g urea was applied at sowing. Each treatment has four duplicate pots with seven wheat plants in each pot. To avoid human subjective factors, the eight wheat plants were randomly selected for each treatment during the experiments to measure the Cd content in each part of the wheat.
MAN was foliar sprayed twice at each period during the booting, heading, and grain-filling stages. The uniform application of MAN was sprayed onto the surface of the leaves in each pot. The control was sprayed with the same volume of deionized water. To prevent MAN from coming into contact with the roots, we used protective measures in both the hydroponic and potting experiments, while performing multiple uniform sprays to ensure that most of the MAN solution was absorbed on the wheat leaf surface.

2.3. Wheat Seedlings Biomass Measurements and Root Scaning

The wheat seedlings treated for two weeks were harvested and photographed, and then the samples were divided into shoots and roots. The fresh weight (FW) was obtained by weighing the samples immediately, and the dry weight (DW) was measured by drying the sample at 85 °C for at least 48 h until the weight was constant. The morphology of the roots were scanned with an EPSON4990 scanner, and the total length, total surface area, root volume, and average diameter of the roots were determined using WinRhizo (Yiketai, Beijing, China).

2.4. Measurements of Chlorophyll Content and Gas Exchange Parameters

Photosynthetic pigment was determined using spectrophotometry (RC-UV1900) after extraction with 95% ethanol [30]. The second fully stretched leaves from the tops of plants were used to estimate the net photosynthetic rate (Pn), stomatal conductance (Gs), intercellular CO2 concentration (Ci), and transpiration rate (Tr) by a portable photosynthesis system (LiCOR 6400, Lincoln, NE, USA) with a red and blue light leaf chamber [31]. The light intensity was 800 µmol m−2 s−1, the atmospheric CO2 concentration was 400 µmol mol−1, room temperature was set to 25 °C, and air relative humidity was 65 ± 5% at the measuring time of 8:30 a.m. to 11:30 a.m.

2.5. Separation and Subcellular Fractions of Cd in Roots

Fresh plants were soaked in EDTA-Na2 solution for 10 min, washed with deionized water, and then the shoots were cut out. The subcellular fractions of roots for heavy metal analysis were prepared according to the method of Zeng et al. [32]. All the subcellular fractions of the roots were freeze-dried and digested with HNO3/HClO4 (87:13 (v/v)) at 100 °C for 1 h, 120 °C for 1 h, 140 °C for 1 h, 160 °C for 1 h, and 180 °C for 1 h. After liquefying the processed samples in 2% HNO3, the concentrations of Cd were measured by plasma mass spectrometry (ICP-MS, Perkin-Elmer NexION 300X, Waltham, MA, USA).

2.6. Cell Wall Extraction, Fractionation, and Its Components Measurement

Extraction of the crude cell wall materials and subsequent fractionation of the cell wall components were accomplished according to Zhu et al. [33]. The uronic acid content in the pectin and the total polysaccharide content in the cellulose and hemicellulose fractions was determined according to Zhu et al. [34].

2.7. The Chemical Forms of Cd in Wheat Root

The chemical forms of Cd in the wheat were successively extracted according to the method of Su et al. [35]. CdE, CdHAC, CdHCl, CdNaCl, and CdW were extracted by ethanol, acetic acid, hydrochloric acid solution, sodium chloride solution, and deionized water, respectively, and the remaining was the residual Cd form (CdR). To simulate the chemical forms of Cd, the root tissues were analyzed using plasma mass spectrometry (ICP-MS, Perkin-Elmer NexION 300X, Waltham, MA, USA).

2.8. Sample Collection

Fresh plants of the hydroponic culture were soaked in EDTA-Na2 solution for 10 min, washed with deionized water, and divided into shoots and roots. Plants of the potted soil experiments were harvested at maturity after rinsing with deionized water three times. Each sample in a pot was divided into roots, stems, leaves, and spikes, respectively. Samples were dried at 85 °C for at least 48 h until the weight was constant. Spikes were threshed into grain, and the other samples were ground into powder.

2.9. Statistical Analysis

The translocation factors (TFs) and bioconcentration factor (BCF) of the Cd from the soil to the aboveground parts were evaluated as follows: TFroot-stem = Cdstem/Cdroot; TFstem-leaf = Cdleaf/Cdstem; TFstem-grain = Cdgrain/Cdstem; BCF = Cdabove-ground parts/Cdsoil.
Data were analyzed using variance, and the means were compared by Duncan’s multiple comparison test or Student’s t-test where appropriate. Data are shown as the means ± SD of eight biological replicates. Different letters above columns indicate significant difference at p ≤ 0.05 among treatments. Calculations were conducted using SPSS 22.0 software (IBM, Inc., Armonk, NY, USA).

3. Results

3.1. Effects of MAN on Biomass and Growth of Wheat Seedlings under Cd Stress

To identify the effects of foliar spray with different MAN concentrations on wheat seedlings under Cd stress, the biomass and growth components were used as important indicators. MAN significantly increased the length, DW, and FW of roots under Cd stress (Figure 1). When the concentration of MAN was 160 μM, the length, DW, and FW of roots increased by 26.1%, 21.2%, and 29.7%, respectively, in comparison with the wheat exposed to Cd alone. The specific changes of the root system after MAN spraying are presented in Table 2. In the presence of Cd stress alone, the total length, average diameter, surface area, volume, and tips of the roots were significantly reduced compared to the control. These indicators increased with variable degrees after the application of MAN at different concentrations. Compared to the Cd treatment alone, the total length, surface area, volume, average diameter, and tips of the roots were all maximized at 160 μM, and the differences were statistically significant. In the present study, it seems that the moderate 160 μM concentration of MAN was best for alleviating Cd stress (Figure 1A,C,D,F,G).

3.2. Effects of MAN on Cd Uptake by Wheat

To further clarify the effect of foliar spraying of MAN on reducing the Cd concentration in wheat, we measured the Cd accumulation levels of shoots and roots. The Cd concentrations in shoots and roots were 0.29 mg g−1 (DW) and 2.55 mg g−1 (DW), respectively (Figure 2). While the foliar spraying of different MAN concentrations significantly promoted Cd uptake of roots compared to Cd treatment alone, up to a 19.7% increase in Cd was observed in the 160 μM MAN treatment. Curiously, the Cd concentration in the shoots did not increase with an increase in the Cd concentration in the roots. However, it showed a significant decrease compared to Cd treatment alone, especially at 160 μM, where the reduction was 16.4%. Therefore, we used a treatment of 160 μM MAN to study the role of MAN in alleviating Cd-induced wheat growth inhibition.

3.3. Effects of MAN on Photosynthetic Pigments and Gas Exchange Parameters

Compared with the control, the content of carotenoids, chlorophyll a, chlorophyll b, and total chlorophyll in leaves under Cd stress were decreased by 37.8%, 41.4%, 41.2%, and 40.8%, respectively. After the application of MAN, the decline was reversed at 22.9%, 23.3%, 14.9%, and 21.7%, respectively (Figure 3A–D). The Pn, Gs, and Tr under Cd stress decreased by 31.7%, 68.3%, and 56.3%, respectively. Compared with the Cd treatment alone, foliar spraying of MAN contributed to an amelioration in the net photosynthetic rate (27.3%), transpiration rate (41.9%), and stomatal conductance (30.0%) (Figure 3E–H).

3.4. Effects of MAN on the Cd Subcellular Distribution of Wheat Roots

To investigate how the application of MAN affects Cd transfer, we first analyzed the subcellular distribution of Cd in the roots of wheat under Cd stress. The subcellular distribution of Cd was mainly in the cell wall (FI), plastids (FII), nucleus (FIII), mitochondria (FIV), and soluble fraction (FV). The results showed that foliar spraying of MAN changed the subcellular distribution of Cd in wheat root (Figure 4). After the application of MAN, the Cd content was increased in the cell wall of the roots and decreased in the soluble components, while the Cd content of the nucleus, mitochondria, and plastids remained basically unchanged. Importantly, the proportion of Cd in the soluble components decreased by 13.9%; however, the proportions of Cd in the cell wall fractions increased by 15.5% with MAN treatment compared to the Cd treatment alone. These results indicate that MAN was conducive to facilitate Cd immobilization and reduced its cellular toxicity, since Cd in the organelle and soluble fractions are highly toxic and mostly bioavailable.

3.5. Effects of MAN on the Cell Wall Composition and Cd Content in Wheat Roots

It is logical that the cell walls of roots are the first barrier to restrict Cd into the cell, because it is the first organ to touch Cd in the growth medium [33]. In the absence of Cd, compared with the control, the application of MAN did not cause significant changes in the content of these components. Moreover, the contents of pectin, cellulose, and hemicellulose in the cell wall of the roots were not changed by Cd stress (Figure 5). Compared to Cd treatment alone, foliar spraying of MAN significantly enhanced both the hemicellulose content and amount of Cd in the hemicellulose. By contrast, the application of MAN had virtually no effect on the cellulose and pectin content. The content of Cd in the pectin and cellulose was basically unchanged, and the increase in the total Cd content in the roots was mainly caused by the increase in Cd accumulation in the hemicellulose.

3.6. Effects of MAN on the Chemical Forms of Cd in Wheat Roots

We then determined the content of various Cd chemical forms in wheat roots under Cd stress (Table 3). The chemical forms of Cd in the roots were predominantly Cde and Cdw. The MAN treatment significantly decreased the Cde and Cdw content in the roots by approximately 13.2% and 6.4%, respectively; by contrast, it significantly increased the content of CdHAc and CdHCl by approximately 51.2% and 54.3%, respectively, compared to the Cd treatment alone. The MAN treatment had a slight influence on the content of CdNaCl and CdR. These results suggest that MAN may lead to more fixation of Cd in the roots, while less Cd was transported to the shoots.

3.7. Effect of MAN on TF and BCF Values of Cd in Wheat

MAN treatment significantly reduced the Cd concentration in the grain by 26.3% and increased the Cd concentration in the roots by 18.0%; however, no significant changes in Cd concentration were observed in the stems and leaves (Table 4). The TF and BCF values depend on the values of Cd concentrations in the soil and various wheat parts. The Cd content, TF, and BCF values among the different parts of wheat are shown in Table 5. In the present study, the order of Cd content in different parts of the wheat was root > stem > leaf > grain; foliar spraying of MAN did not alter this order. The Cd translocation from stems to leaves was the highest with or without MAN application, measuring 0.64 and 0.62, respectively. Interestingly, the values of TFroot-stem, TFstem-leaf, and TFleaf-grain were reduced by 25.0%, 3.1%, and 18.0%, respectively, with foliar MAN spraying; in fact, TFroot-stem decreased significantly. The BCF values for Cd were ordered as roots > leaves > stems > grain in the two treatments. Foliar spraying of MAN caused a 10.2, 10.7, and 16.7% decrease in BCFstem, BCFleaf, and BCFgrain, but it caused a 17.5% increase in BCFroot compared with the control; the changes in BCFroot and BCFgrain were significant.

4. Discussion

It was found that carbon atoms derived from labeled exogenous MAN can be detected in ascorbic acid of Arabidopsis thaliana. As a substrate, MAN is synthesized as ascorbic acid through the D-mannose/L-galactose pathway and enters the AsA-GSH cycle to participate in stress response [36]. Exogenous MAN treatment restores the Cd-sensitive phenotype of endonucleated-β-mannanase gene (xcd1-2) mutants in Arabidopsis thaliana and improves the tolerance of wild-type plants to Cd. MAN regulates the expression of chelated peptide biosynthetic pathway-related genes in Arabidopsis thaliana under Cd stress to increase the chelated peptide content [37]. Among the proteins regulated by MAN in wheat under Cd stress, there are five differential proteins: GSTF1, GSTU1, GSTU6, GSTZ5, and P0043B10.43. Foliar spraying of MAN can improve wheat Cd tolerance by increasing the glutathione content, enhancing reactive oxygen species scavenging ability, and reducing oxidative stress [10]. It has been widely demonstrated that high-concentration MAN can modify the antioxidant system of wheat [25,38]. Recently, there have been fewer studies of the enhancement of Cd stress tolerance by foliar spraying with MAN. In the present study, we elucidated the possible mechanisms by which MAN decreases the accumulation of Cd in wheat grain through photosynthesis, subcellular distribution, and the chemical forms of Cd.

4.1. MAN Alleviated Cd Stress in Wheat

Cd toxicity can reduce the shoot height and root depth of wheat plants, and cause a reduction in shoot and root biomass [39,40,41,42]. In this study, we observed that the growth of wheat was adversely affected by Cd stress. It has been reported that MAN treatment increased the length and FW of Arabidopsis roots exposed to Cd, but it had no effect on the shoots [43]. We obtained similar results in wheat, and in addition, MAN increased the DW of wheat roots exposed to Cd. Various MAN concentration treatments (except for 640 μM) had mitigation effects on these inhibitions caused by Cd stress, and a moderate concentration (160 μM) showed the optimal effects. Our results showed that Cd stress caused Cd accumulation in wheat compared to the control. However, foliar spraying of MAN decreased Cd retention in the shoots and increased Cd accumulation in the roots of wheat, and the greatest reduction in Cd in the shoots was seen at 160 μM. Thus, we selected this concentration for further study.
The concentration of chlorophyll a, chlorophyll b, and carotenoid in wheat leaves would decrease due to Cd exposure [44,45]. Cd also can decrease the Pn, Tr, and Gs of wheat [28,46,47]. In the present study, we also found that Cd stress caused an obvious decrease in these indicators. However, compared with Cd treatment alone, foliar spraying with MAN significantly increased the chlorophyll a content, chlorophyll b content, total chlorophyll content, carotenoid content, and Pn, Gs, and Tr of wheat leaves under Cd stress. These results suggested that foliar spraying of MAN reduced the damage of Cd to the photosynthetic apparatus of wheat leaves.

4.2. MAN Can Enhance Cd Accumulation in the Cell Wall

Many studies found that most heavy metals accumulated in the roots, with only a few entering the plant’s aboveground parts [48]. The extracellular body, composed of the cell wall and intercellular layer, is the first barrier to prevent the entry of toxic heavy metals into the protoplasts. Fixing of Cd in the cell wall would contribute to decreasing the available Cd that can be transported into the cell. Deposition in the cell wall is one of the main ways for many plants to decrease Cd toxicity [49]. Once Cd is transported into the cytosol, it is partitioned among various cytosolic ligands and intracellular organelles, where it can cause potentially adverse effects [50]. Previous reports have found that sodium hydrosulfide (NaHS) treatment enhances a plant’s tolerance to Cd by inactivating Cd and isolating it into the cell wall [51]. Interestingly, with the MAN treatment, the proportion of Cd content in the soluble, plastid, nucleus, and mitochondrial fractions of the roots did not change obviously, compared with those plants without MAN treatment, but the total Cd content decreased significantly (Figure 4). However, MAN treatment significantly increased the proportion of Cd in the cell wall fraction by approximately 16.0%. These results showed that foliar spraying of MAN increased the potential of the cell wall to fix Cd.

4.3. MAN Enhanced the Cd-Binding Capacity of Hemicellulose

Cell wall polysaccharides mainly include cellulose, hemicellulose, and pectin. The groups on the cell wall polysaccharides can immobilize heavy metals [52]. Carboxyl, aldehyde, amino, phosphate, and other negatively charged groups can affix metal cations to the cell wall by various reactions to reduce the entry of heavy metal ions into the cytoplasm [53]. Many studies have shown that a change in the polysaccharide content can alter the adsorption of heavy metal ions and the growth of plants, which serves as an adaptive response to heavy metal stress. For example, exogenous NO increases the pectin and hemicellulose content in the root cell wall of rice, which increases the accumulation of Cd there, and reduces the soluble Cd content in the leaves [54]. In the absence of phosphorus, the content of hemicellulose in the root cell walls of Arabidopsis thaliana decreased, resulting in a decrease in the amount of Cd retained in the cell walls [34]. In addition, the exogenous auxin treatment of Arabidopsis can promote an increase in the hemicellulose 1 content in root cell walls, leading to an increase in Cd retention in the root cell wall, thus reducing the transport of Cd to the shoots [33]. In the present study, the MAN treatment significantly enhanced both the hemicellulose content and the amount of Cd in the hemicellulose, compared to Cd alone (Figure 5). However, foliar spraying of MAN had little effect on the pectin and cellulose content. Moreover, the proportion of Cd in the pectin and cellulose did not change significantly. These results indicate that hemicellulose is the main contributor to the increase in Cd retention in the cell wall fraction of the roots with MAN treatment.

4.4. MAN Alters the Chemical Forms of Cd

The chemical forms’ distribution of Cd in plants is directly related to its activity, toxicity, and migration ability [55]. CdNaCl is the form that can combine with protein, which interferes with enzyme activity and affecting the normal growth and development of crops. The higher proportion of Cde, Cdw, and CdNaCl forms, the lower tolerance of plants to Cd stress [56]. Studies have shown that the difference in the chemical form distribution of Cd in wheat varieties with low Cd accumulation and high Cd is an important factor affecting the Cd content in wheat grain [57]. There are two parallel pathways for Cd transport from the root to shoot, including active transport in the symplast and passive transport though the apoplast (i.e., cell wall) [58,59]. In this study, foliar spraying of MAN significantly increased CdHAc and CdHCl in roots, which were not easily transferred to the aboveground part of wheat via the symplast pathway. The addition of exogenous substances may alter the chemical forms of Cd in wheat by regulating the expression levels of Cd transporter gene and phytochelatin synthase gene [56,60].

4.5. MAN Inhibits Cd Transport into the Above-Ground Parts

BCF and TF are important parameters for evaluating the ability of Cd to accumulate and transfer in plants, and they are often used to characterize heavy metal migration and predict Cd concentrations in plant tissues [61,62]. The content of Cd, pH, organic matter, cation exchange, and clay content in the soil all affected the BCF and TF of wheat [63,64]. The decrease in Cd BCF and TF in plants tends to be synergistic with different pathways [65]. Some studies indirectly changed the soil physicochemical properties by adding exogenous substances to the soil to reduce the BCF and TF of wheat [61,63]. In the present study, foliar spraying of MAN had a significant impact on Cd accumulation and absorption by decreasing the TFroot-stem, TFstem-leaf, and TFleaf-grain values. This may be due to the MAN treatment increasing the ability of the cell wall to immobilize Cd, which effectively prevents the upward transfer of Cd in wheat.

5. Conclusions

We found that foliar spraying of 160 μM MAN significantly alleviated the inhibition of photosynthetic capacity and root growth of wheat seedlings induced by Cd stress. Compared with Cd treatment alone, foliar spraying of MAN significantly reduced the Cd content in the shoots and increased the Cd content in the roots of wheat seedlings. Foliar spraying of MAN increased the hemicellulose content in the cell wall of wheat roots, and more Cd was trapped in the cell wall, which reduced the amount of Cd entering the protoplast. Compared with Cd treatment alone, foliar spraying of MAN changed the distribution of the Cd’s chemical forms in wheat roots and significantly increased the content of CdHAc and CdHCl, with weak migration ability. The results of the potted soil experiments showed that, compared with the control, foliar spraying of 160 μΜ MAN significantly reduced the Cd concentration of wheat grain by 26.3%. In conclusion, foliar spraying of MAN increased the retention of Cd in wheat roots and inhibited the transport of Cd from roots to shoots (Figure 6).

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy12102273/s1, Table S1: Effects of different concentrations of Cd on the growth of wheat seedlings.

Author Contributions

Conceptualization, X.C. and N.P.; methodology, W.H.; software, X.Z.; validation, L.S.; formal analysis, X.C.; investigation, N.P.; resources, L.S.; data curation, X.Z.; writing—original draft preparation, X.Z.; writing—review and editing, X.Z. and W.L.; visualization, X.Z. and W.L.; supervision, X.Z. and W.L.; project administration, X.Z. and W.L.; funding acquisition, W.L. 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 (2016YFD0800700).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data sharing not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02273 g001 550
Figure 1. Effects of different concentration of MAN on wheat (A); plant height (B); root depth (C); FW of shoot (D); DW of shoot (E); FW of root (F) and DW of root (G) under Cd stress. One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0, 40, 80, 160, 320, or 640 µM MAN for two weeks. Data are the means ± SD and different letters above columns indicate a significant difference at p ≤ 0.05 among treatments.
Figure 1. Effects of different concentration of MAN on wheat (A); plant height (B); root depth (C); FW of shoot (D); DW of shoot (E); FW of root (F) and DW of root (G) under Cd stress. One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0, 40, 80, 160, 320, or 640 µM MAN for two weeks. Data are the means ± SD and different letters above columns indicate a significant difference at p ≤ 0.05 among treatments.
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Figure 2. Effects of different concentrations of MAN on Cd accumulation in shoots (A) and roots (B) of wheat seedlings under Cd stress. One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0, 40, 80, 160, 320, or 640 µM MAN for two weeks. Data are the means ± SD and different letters above columns indicate a significant difference at p ≤ 0.05 among treatments.
Figure 2. Effects of different concentrations of MAN on Cd accumulation in shoots (A) and roots (B) of wheat seedlings under Cd stress. One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0, 40, 80, 160, 320, or 640 µM MAN for two weeks. Data are the means ± SD and different letters above columns indicate a significant difference at p ≤ 0.05 among treatments.
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Figure 3. Effects of MAN on the chlorophyll a content (A); chlorophyll b content (B); total chlorophyll content (C); carotenoids content (D); net photosynthetic rate (E); intercellular CO2 concentration (F); transpiration rate (G); and stomatal conductance (H) in wheat leaves under Cd stress. One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0 or 160 µM MAN for two weeks. Data are the means ± SD and different letters above columns indicate a significant difference at p ≤ 0.05 among treatments.
Figure 3. Effects of MAN on the chlorophyll a content (A); chlorophyll b content (B); total chlorophyll content (C); carotenoids content (D); net photosynthetic rate (E); intercellular CO2 concentration (F); transpiration rate (G); and stomatal conductance (H) in wheat leaves under Cd stress. One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0 or 160 µM MAN for two weeks. Data are the means ± SD and different letters above columns indicate a significant difference at p ≤ 0.05 among treatments.
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Figure 4. Effect of MAN on the Cd concentration (A), and the subcellular distribution of Cd (B,C) in wheat roots. One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0 or 160 µM MAN for two weeks.
Figure 4. Effect of MAN on the Cd concentration (A), and the subcellular distribution of Cd (B,C) in wheat roots. One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0 or 160 µM MAN for two weeks.
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Agronomy 12 02273 g005a 550Agronomy 12 02273 g005b 550
Figure 5. Effects of MAN on the cellulose content (A); the total sugar residues content in hemicellulose (B); the pectin content, calculated as Gal A in the cell wall of wheat roots under Cd stress (C); the Cd content in the cell wall component of wheat roots (D–F). One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0 or 160 µM MAN for two weeks. Data are the means ± SD and different letters above columns indicate a significant difference at p ≤ 0.05 among treatments.
Figure 5. Effects of MAN on the cellulose content (A); the total sugar residues content in hemicellulose (B); the pectin content, calculated as Gal A in the cell wall of wheat roots under Cd stress (C); the Cd content in the cell wall component of wheat roots (D–F). One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0 or 160 µM MAN for two weeks. Data are the means ± SD and different letters above columns indicate a significant difference at p ≤ 0.05 among treatments.
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Figure 6. The working mode of MAN-enhanced Cd tolerance of wheat under Cd stress.
Figure 6. The working mode of MAN-enhanced Cd tolerance of wheat under Cd stress.
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Table
Table 1. Basic properties of the experimental topsoil (0–20 cm).
Table 1. Basic properties of the experimental topsoil (0–20 cm).
Soil PropertiesValue (Pot)
pH7.02
Organic matter (g kg−1)14.80
Alkali N (mg kg−1)36.05
Available P (mg kg−1)30.15
Available K (mg kg−1)87.12
Total Cd (mg kg−1)3.30
EDTA-Cd (mg kg−1)1.71
Table
Table 2. Effects of different concentration of MAN on wheat total length, surface area, volume, average diameter, and tips under Cd stress.
Table 2. Effects of different concentration of MAN on wheat total length, surface area, volume, average diameter, and tips under Cd stress.
TreatmentLength (cm)Surface Area (cm2)Root Volume (cm3)Average
Diameter (mm)		Tips
Con349 ± 5.32 a16.2 ± 0.59 a0.098 ± 0.0003 a0.242 ± 0.008 a2423 ± 9.81 a
Cd165 ± 8.19 c10.7 ± 0.84 c0.055 ± 0.0061 d0.206 ± 0.006 d1584 ± 33.4 cd
Cd + 40 Man167 ± 15.1 c11.8 ± 1.30 bc0.067 ± 0.0088 cd0.225 ± 0.007 bc1694 ± 149.7 bcd
Cd + 80 Man207 ± 16.9 b13.7 ± 0.97 ab0.072 ± 0.0043 c0.211± 0.002 cd1553 ± 67.1 c
Cd + 160 Man207 ± 4.68 b15.2 ± 0.41 a0.089 ± 0.0052 ab0.234 ± 0.002 ab1982 ± 50.9 b
Cd + 320 Man210 ± 20.9 b14.5 ± 1.20 ab0.080 ± 0.0052 bc0.221± 0.004 bcd2023 ± 185.7 b
Cd + 640 Man155 ± 1.47 c10.1 ± 0.29 c0.052 ± 0.0023 d0.207 ± 0.004 d1875 ± 210.2 bcd
Note: one-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0, 40, 80, 160, 320, or 640 µM MAN for two weeks. Data are shown as the means ± SD and different letters indicate significant differences by Duncan’s multiple comparison test (p ≤ 0.05).
Table
Table 3. Effect of MAN on the chemical forms of Cd in wheat roots under Cd stress.
Table 3. Effect of MAN on the chemical forms of Cd in wheat roots under Cd stress.
TreatmentCdE
(mg kg−1)		CdW
(mg kg−1)		CdNaCl
(mg kg−1)		CdHAC
(mg kg−1)		CdHCl
(mg kg−1)		CdR
(mg kg−1)
Cd543.1 ± 29.5870.9 ± 20.5410.8 ± 21.6329.8 ± 25.2238.6 ± 32.9111.1 ± 13.7
Cd + Man471.1 ± 28.6 *815.0 ± 19.4 *458.4 ± 33.2498.8 ± 22.2 *368.2 ± 32.8 *140.9 ± 21.2
Data are shown as the means ± SD, and * represents a significant difference compared to the control group, calculated by Student’s t-test (p ≤ 0.05). One-week-old wheat seedlings under 20 μM CdCl2 were sprayed with 0 or 160 µM MAN for two weeks.
Table
Table 4. Effects of MAN on the Cd content in different parts of wheat in potted soil experiments.
Table 4. Effects of MAN on the Cd content in different parts of wheat in potted soil experiments.
TreatmentRoot Cd
Content
(mg kg−1)		Stem Cd
Content
(mg kg−1)		Leaf Cd
Content
(mg kg−1)		Grain Cd
Content
(mg kg−1)
Con8.73 ± 0.46 2.76 ± 0.20 1.75 ± 0.18 0.19 ± 0.02
MAN10.3 ± 0.59 *2.46 ± 0.07 1.57 ± 0.06 0.14 ± 0.01 *
Note: Data are shown as the means ± SD, and * represents a significant difference compared to the control group, calculated by Student’s t-test (p ≤ 0.05).
Table
Table 5. Effects of MAN on the Cd transport and bioconcentration in potted soil experiments.
Table 5. Effects of MAN on the Cd transport and bioconcentration in potted soil experiments.
TreatmentTFroot-stemTFstem-leafTFleaf-grainBCFrootBCFleafBCFstemBCFgrain
Con0.32 ± 0.03 0.64 ± 0.06 0.11 ± 0.02 2.79 ± 0.15 0.88 ± 0.06 0.56 ± 0.06 0.06 ± 0.01
MAN0.24 ± 0.02 *0.62 ± 0.05 0.09 ± 0.01 *3.28 ± 0.19 *0.79 ± 0.05 0.50 ± 0.19 0.05 ± 0.00 *
Note: Data are shown as the means ± SD, and * represents a significant difference compared to the control group, calculated by Student’s t-test (p ≤ 0.05).
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Zheng, X.; Cheng, X.; Pan, N.; Huang, W.; Shi, L.; Lu, W. Foliar Spraying of Mannose Alleviates Cadmium Stress by Changing the Subcellular Distribution and Chemical Forms of Cadmium in Wheat Root. Agronomy 2022, 12, 2273. https://doi.org/10.3390/agronomy12102273

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Zheng X, Cheng X, Pan N, Huang W, Shi L, Lu W. Foliar Spraying of Mannose Alleviates Cadmium Stress by Changing the Subcellular Distribution and Chemical Forms of Cadmium in Wheat Root. Agronomy. 2022; 12(10):2273. https://doi.org/10.3390/agronomy12102273

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Zheng, Xiang, Xue Cheng, Ni Pan, Wei Huang, Liang Shi, and Wei Lu. 2022. "Foliar Spraying of Mannose Alleviates Cadmium Stress by Changing the Subcellular Distribution and Chemical Forms of Cadmium in Wheat Root" Agronomy 12, no. 10: 2273. https://doi.org/10.3390/agronomy12102273

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