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Article

The Mechanism of an Fe-Based MOF Material as a Foliar Inhibitor and Its Co-Mitigation Effects on Arsenic and Cadmium Accumulation in Rice Grains

by
Tianyu Wang
1,2,
Hao Cui
3,
Weijie Li
3,
Zhenmao Jiang
1,
Lei Li
1,
Lidan Lei
1,2,* and
Shiqiang Wei
1,*
1
Department of Environment Science and Engineering, College of Resources and Environment, Southwest University, Chongqing 400715, China
2
Chongqing Jinfo Mountain Karst Ecosystem National Observation and Research Station, School of Geographical Sciences, Southwest University, Chongqing 400715, China
3
Sichuan Provincial Key Laboratory of Philosophy and Social Sciences for Monitoring and Evaluation of Rural Land Utilization, Chengdu Normal University, Chengdu 611130, China
*
Authors to whom correspondence should be addressed.
Agronomy 2025, 15(7), 1710; https://doi.org/10.3390/agronomy15071710
Submission received: 27 May 2025 / Revised: 4 July 2025 / Accepted: 14 July 2025 / Published: 16 July 2025
(This article belongs to the Topic Effect of Heavy Metals on Plants, 2nd Volume)
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Abstract

Arsenic (As) and cadmium (Cd) in rice grains are major global food safety concerns. Iron (Fe) can help reduce both, but current Fe treatments suffer from poor stability, low leaf absorption, and fast soil immobilization, with unclear underlying mechanisms. To address these issues, an Fe-based metal–organic framework (MIL-88) was modified with sodium alginate (SA) to form MIL-88@SA. Its stability as a foliar inhibitor and its leaf absorption were tested, and its effects on As and Cd accumulation in rice were compared with those of soluble Fe (FeCl3) and chelating Fe (HA + FeCl3) in a field study on As–Cd co-contaminated rice paddies. Compared with the control, MIL-88@SA outperformed or matched the other Fe treatments. A single foliar spray during the tillering stage increased the rice yield by 19% and reduced the inorganic As and Cd content in the grains by 22.8% and 67.8%, respectively, while the other Fe treatments required two sprays. Its superior performance was attributed to better leaf affinity and thermal stability. Laser ablation inductively coupled plasma–mass spectrometry (LA–ICP–MS) and confocal laser scanning microscopy (CLSM) analyses revealed that Fe improved photosynthesis and alleviated As–Cd stress in leaves, MIL-88@SA promoted As and Cd redistribution, and Fe–Cd co-accumulation in leaf veins enhanced Cd retention in leaves.

1. Introduction

The U.S. Department of Agriculture’s Supply and Demand Report for September 2023 states that global rice consumption has reached 522.7 million tons, with China accounting for 30% of total consumption. Rice tends to accumulate high levels of As and Cd in its grains, posing serious health risks to people consuming rice as a staple food [1]. As and Cd are phytotoxic, even at low concentrations, and can be readily transferred from contaminated soil into plants and threaten human health [2,3]. However, the simultaneous reduction in As and Cd levels in rice grains is a challenge because of their opposite geochemical behaviors in paddy soils [4]. Therefore, new strategies are needed to ensure safe rice production in As–Cd co-contaminated paddy soil.
Currently, practical strategies to mitigate the accumulation of As and Cd in rice that have been implemented include water management [5], phytoremediation [6], in situ passivation [7], and foliar inhibition [8]. Among these techniques, in situ passivation and foliar inhibitor application are more practically feasible and are frequently used at the field scale. In situ passivation may effectively reduce the bioavailability of As and Cd in soils if it is suitable [9]. However, effective and low-cost passivators with dual roles suppressing the bioavailability of both As and Cd are rare. Moreover, the long-term effects of passivators on heavy metal immobilization in contaminated soil remain unclear, and there is a risk that heavy metals will be released over time [10,11]. Compared with in situ passivation, foliar spraying of heavy metal inhibitors has several advantages. These substances can be directly absorbed by crop leaves and mitigate heavy metals without potentially adverse effects on soil properties. Moreover, drone spraying can be used to facilitate application in large-scale rice production. The effectiveness of foliar inhibitors containing elements such as Si, Se, Zn, and Fe in reducing heavy metal accumulation in crops has been verified by numerous studies [12,13,14,15]. However, previous studies focused primarily on the control of a single toxic element. For example, Zhen [16] reported that foliar spraying of a ZnSO4 solution twice at the rice filling stage reduced the Cd content in rice grains by 32.3%. Similarly, Zhang et al. [17] reported that spraying Na2SiO3 solution twice at the rice tillering stage decreased the inorganic arsenic (iAs) content in rice grains by 20.9%. Foliar inhibitors aimed at reducing the concentrations of multiple toxic heavy metals are still scarce.
In addition, the efficiency of foliar inhibitors may be affected by their affinity for crop leaves. Most foliar inhibitors exist in water-soluble form and may not be well retained on rice leaves because of the hydrophobic lipid layer in the leaf cuticle. Approximately 50% of nutrients and over 95% of pesticides sprayed on crops never reach their target and are wasted [18]. Moreover, the efficacy of foliar inhibitors is concentration-dependent. High concentrations may cause mesophyll cell scorching and affect plant photosynthesis, whereas low concentrations may be ineffective [19]. To overcome these limitations, the use of nanoparticles (NPs) has recently emerged as an efficient and promising approach. NPs are more easily retained on the leaf surface. The small particle size enables them to readily penetrate leaf tissues and release nutrients to the crop constantly throughout growth [20]. Previous studies have demonstrated that foliar inhibitors in the NP form, such as ZnO-NPs, SiO2-NPs, and CeO2-NPs, are more effective at improving crop quality and protecting plants from heavy stress than those in water-soluble forms [21,22]. For example, Chen et al. [23] reported that foliar application of nano-SiO2 reduced Cd concentration in grains by 31.6–61.9% and promoted the translocation of K, Mg, and Fe in rice plants. However, NPs possess unique physical and chemical properties because of their large surface area and nanoscale size; thus, the potential toxicity of these particles is unknown [24]. Therefore, it is essential to determine whether a foliar inhibitor exists that combines the advantages of both solutions and NPs to reduce the accumulation of As and Cd in rice grains simultaneously.
Metal–organic frameworks (MOFs) represent a novel category of hybrid porous materials composed of metal cations/clusters and multidentate organic ligands. The remarkable porosity, adjustable structure, and multiple metal sites of these materials allow a wide range of applications, including gas storage, molecular separation, sensing, slow drug release, etc. [25]. Recently, MOFs have been applied in agriculture. For example, ZIF-8 NPs have been used to load pesticides [26]. Our previous study demonstrated the effectiveness of using ZIF-8@Ge-132 as a foliar inhibitor for the co-mitigation of As and Cd in rice grains in contaminated paddy fields. On this basis, MOFs with more environmentally friendly transition metals as the coordination centers are worthy of exploration. Iron (Fe) is the fourth most abundant element on Earth. It is also an essential element for all life. Thus, an Fe-containing MOF (Fe-MOF) could be well suited as a foliar inhibitor. As a type of Fe-MOF, MIL-88 has a stable three-dimensional (3D) framework known for its stability in various chemical reaction systems [27], which could enable the sustainable release of Fe3+/Fe2+ to the plant [28]. To increase the affinity of MIL-88 as a foliar inhibitor for rice leaves, sodium alginate (SA), which is a hydrophilic linear polysaccharide copolymer of D-mannuronic acid (M) and L-guluronic acid (G) derived from brown seaweed and bacteria, can be used as a cross-linking agent [29]. The polar groups of the SA chains (e.g., OH, COO-, and short chains) may combine with the wax layer on the leaf surface, thus increasing the affinity of MIL-88 for rice leaves.
In this work, a novel foliar inhibitor consisting of an Fe-MOF crosslinked with SA, designated MIL-88@SA, was fabricated via a simple reaction system, and its basic properties were characterized. Its efficacy in simultaneously mitigating arsenic and cadmium accumulation in rice grains was evaluated in a co-contaminated paddy field, with FeCl3 and FeCl3 + HA as controls. Using CLSM and LA–ICP–MS, the spatial distribution and redistribution of As and Cd in rice tissues were elucidated, enabling the proposal of the underlying inhibitory mechanisms of MIL-88@SA. This technology offers an efficient, eco-friendly approach to mitigate heavy metal contamination, which has the potential to improve crop safety and sustainability in agriculture.

2. Materials and Methods

2.1. Preparation of MIL-88@SA

Briefly, 0.27 g of FeCl3·6H2O (Sinopharm Chengdu Pharmaceutical Co., Ltd., Chengdu, China) and 0.4 g of C8H6O4 (terephthalic acid) (Sinopharm Chengdu Pharmaceutical Co., Ltd., Chengdu, China) were dissolved in 27 mL of N, N-dimethylformamide (DMF) (Merck KGaA., Shanghai, China); then, 3 mL of triethylamine (Merck KGaA., Shanghai, China) was rapidly poured into the mixed solution, which was placed in a Teflon-lined stainless-steel autoclave (Bositai, Chengdu, China) at 180 °C for 12 h. The obtained dark orange solid was centrifuged and purified three times with DMF and ethanol, after which it was immersed in methyl alcohol (Sinopharm Chengdu Pharmaceutical Co., Ltd., Chengdu, China) for 3 days. The fresh MIL-88 was dried overnight at 70 °C under vacuum. Afterward, the MIL-88 was transferred into 0.2% (w/v) SA solution under magnetic stirring for 30 min. Then, 0.5% (w/v) CaCl2 (Sinopharm Chengdu Pharmaceutical Co., Ltd., Chengdu, China) solution was slowly dropped into the SA/MIL-88 mixed solution for crosslinking for 1 h. Finally, MIL-88@SA was obtained after the material was rinsed with deionized water several times to remove the residual curing agent solution and freeze-dried for 24 h.

2.2. Experimental Site

The experimental site was located in Chi Zhou city (E 117°29′44″, N 30°40′27″), Anhui Province, China. The soil type in the region is red loam. The local climate is humid subtropical with an average annual temperature and precipitation of 16.8 °C and 1377 mm, respectively, which are favorable for rice production. The basic soil physicochemical properties are given in Table 1. The soil was classified as slightly acidic, with a pH of 6.02, as determined using the national standard method (HJ 962-2018), and was co-contaminated with Cd (0.72 mg/kg) and As (18.24 mg/kg) at concentrations exceeding the risk screening criteria of the Chinese Soil Environmental Quality Standard (GB 15618-2018).

2.3. Experimental Design

The field experimental rice variety used was “YLY 1998”, which has been recommended by the Anhui Academy of Agricultural Sciences for local cultivation. After the soil was plowed thoroughly, the experimental field was partitioned into 12 plots with areas of 3 × 5 m2. Four foliar application treatments were designed: CK (only sprayed with deionized water), FeCl3, FeCl3 + HA, and MIL-88@SA, which were recorded as S1, S2, S3, and S4, respectively. The spray concentrations of all the Fe-containing agents were set to 1% (w/v), in agreement with Wang et al. [14]. Each treatment was replicated across three separate plots and arranged randomly. All cultural practices and basic fertilizer application procedures (500 kg·ha−1 of N, P, and K combined fertilizer, N:P2O5:K2O = 10:5:13) were the same for each plot throughout the experiment. Rice seedlings were transplanted into the plots in a planting arrangement of 15 × 20 cm, on 28 May 2023. In the S2 and S3 groups, foliar spraying was performed twice on a cloudy and humid morning (9:00–11:00 a.m.) at the rice tillering and flowering stages. The S4 group was sprayed only once at the tillering stage. Fresh rice plant tissues, including roots, stems, leaves, and grains, were collected at harvest and washed with deionized water; half of these materials were immediately stored at −80 °C for tissue visualization and elemental distribution mapping by CLSM and LA–ICP–MS. The remaining plant tissues from each treatment were dried at 40 °C for 72 h for further analysis of As, Cd, and Fe contents. In this study, the basic physiochemical properties of the soil were determined in accordance with the national Risk Control Standard for Soil Contamination of Agricultural Land (Trial) (GB 15618-2018), ensuring the scientific validity and comparability of the data. The specific parameters measured included the soil pH, organic matter content (%), total nitrogen (g·kg−1), total phosphorus (g·kg−1), available potassium (mg·kg−1), and cation exchange capacity (CEC, cmol·kg−1).

2.4. Analytical Methods

2.4.1. Determination of the As and Cd Contents in the Soil

To determine the total As and Cd, approximately 50 mg of soil powder (<200 mesh) was accurately weighed into a Teflon digestion vessel and moistened with ultrapure water. Then, 1.0 mL of HNO3 and 1.0 mL of HF were added. The sealed vessel was heated at 190 °C for over 48 h. After cooling, the solution was evaporated to dryness at approximately 120 °C, followed by the addition of 1 mL HNO3 and a second evaporation to dryness. The residue was re-dissolved in 3 mL of 30% HNO3, resealed, and heated again at 190 °C for more than 12 h. Finally, the digested solution was diluted to approximately 100 g with 2% HNO3 and analyzed via coupled plasma mass spectrometry (ICP-MS) [30].
The DTPA-extractable concentrations of As and Cd in the soil were determined using the DTPA extraction method. The air-dried and sieved soil samples were shaken with a DTPA extraction solution (0.005 mol/L DTPA, 0.01 mol/L CaCl2, and 0.1 mol/L triethanolamine, pH 7.3) for 120 min. After extraction, the suspension was filtered, and the concentrations of As and Cd in the filtrate were measured via ICP–MS.

2.4.2. Methods for Determining the Structure and Properties of MIL-88@SA

The surface morphology of MIL-88@SA was characterized via transmission electron microscopy (TEM, JEOL Ltd., Tokyo, Japan), and the chemical structures of MIL-88 and MIL-88@SA were examined via powder X-Ray diffraction (XRD, Bruker, Germany) with Cu Kα radiation (λ = 1.5418 Å) and a 2-theta range from 5° to 40°. Fourier transform infrared spectroscopy (FTIR, Thermo Scientific, Waltham, MA, USA) and X-Ray photoelectron spectroscopy (XPS, ESCALAB 250Xi, Waltham, MA, USA) were employed to analyze the functional groups and elemental distribution of MIL-88@SA, respectively. The thermal stability was determined by thermogravimetry (TG, PerkinElmer, Waltham, MA, USA).

2.4.3. Methods for the Analysis of Plants in the Field Experiment

The digested plant samples were subjected to ICP–MS (PerkinElmer NexION 350D, Waltham, MA, USA) for determination of As, Cd, Fe, and micronutrients [31]. The detailed procedures are available in the Supplementary Materials (Text S1). All the analyses were repeated three times. The frozen roots, stems, and leaves were cut very thin by hand, and Fluorol Yellow 088 was added; the colored plant tissues were observed using CLSM [32]. The chlorophyll content of the rice leaves was determined using a SPAD-502 chlorophyll meter (Konica Minolta, Osaka, Japan). All chemicals involved were of guaranteed grade.
Plant tissue microscopic imaging via LA–ICP–MS was developed as the method of choice for elemental imaging of thin sections of biological tissue. The analytical data were quantified by standard reference materials (SRMs) (e.g., tomato leaf SRM NIST 1573a) or synthetic matrix-matched laboratory standards via a preparation procedure similar to that described in some reports [33].
NIST1573a was applied to standard substances for single-point calibration, and the contents of 111Cd, 75As, and 57Fe were 1.517 mg/kg, 0.1126 mg/kg, and 367.5 mg/kg, respectively. 13C was confirmed as an effective internal standard element for calibrating different ablation experiments and water quantities [34]. Figure S2 shows the standard calibration of the target elements. LA–ICP–MS measurements were performed on an ArF excimer 193 nm laser ablation system coupled to a high-resolution ICP-MS instrument (ELEMENT2-XR, Thermo Scientific, Waltham, MA, USA). NIST SRM 610, a silicate glass reference material, was used for conventional tuning to obtain the maximum signal intensity of 238U+, maintain the 238U+/232Th+ ratio close to 1, and ensure low oxide formation (232Th16O+/232Th+ < 0.3%). The detailed operating parameters are summarized in Table S1. Data processing, off-line selection, background integration, and signal analysis were performed using the software ICP-MS DataCal 3.1.

2.5. Data Processing and Statistics

The As and Cd translocation factors (TFs) in the corresponding rice tissues were calculated with the following equations:
TFRoot-stem = Cstem/Croot
TFStem-leaf = Cleaf/Cstem
TFLeaf-grain = Cgrain/Cleaf
TFStem-grain = Cgrain/Cstem
where Cgrain mg/kg, Cleaf mg/kg, Croot mg/kg, Cstem mg/kg, and C ground mg/kg are the contents of Cd and As in the corresponding rice tissues.
The software programs Origin 8.5, Surfer 16, and IBM SPSS Statistics 21 were used for data processing and correlation analysis. Significant differences among treatments were tested using one-way analysis of variance (ANOVA) (Duncan, p ≤ 0.05) or an independent sample t test.

3. Results and Discussion

3.1. Characterization of MIL-88@SA

The morphology of MIL-88@SA illustrated that uniformly spun conical crystals wrapped in an SA layer were successfully prepared with an average size of 211 nm (Figure 1b). The XRD pattern of MIL-88@SA exhibited similar diffraction peaks to the typical peaks of MIL-88 [35]. The FT-IR spectra are shown in Figure 1d. Characteristic absorption peaks of MIL-88 and MIL-88@SA were observed near 1396 and 1656 cm−1, which primarily originated from the asymmetric vibration of the carboxyl group and the symmetric vibration of the carbonyl group. Fe-O-induced bending vibrations in the MOFs were also observed at 516 cm−1, indicating the formation of a metal–carboxylic acid coordination framework [36]. The broad peak at 3200–3500 cm−1 was attributed to the -OH stretching vibration peak in SA. The presence of Fe, C and O in MIL-88@SA, as shown in the XPS spectrum, and the peak at a binding energy of 531 eV in the O 1s spectrum further confirmed the formation of Fe–O–C coordination bonds [37] (Figure S3b). These results indicated that MIL-88@SA was successfully synthesized. The deconvolution of the FeIII 2p3/2 and FeIII 2p1/2 peaks located at 711 and 725 eV, respectively, indicated that Fe3+ existed as an active ion within the self-assembled nanocrystals [38] (Figure 1f). Deconvolution of the Fe peaks in MIL-88@SA indicated that the addition of SA did not alter the chemical environment of Fe3+ compared with that in MIL-88. Instead, the encapsulation of Fe by organic matter and SA endows the material with important physicochemical properties that facilitate its slow release and increase its attachment to the leaf surface [39]. The initial weight loss from the MIL-88@SA was approximately 10% at 100 °C, which may have been attributable to moisture adsorbed on the sample surface. The second weight loss occurred between 100 °C and 500 °C and amounted to approximately 45%; this was attributed to decarboxylation of the organic linker. The third weight loss, which occurred between 500 °C and 700 °C, resulted from the complete decomposition of the framework (Figure S3b). Hence, this thermal stability indicates that MIL-88@SA maintains its structural integrity at room temperature, making it suitable for applications under ambient conditions without decomposition. Although most MOFs are unstable and difficult to apply beyond the laboratory scale, MOFs composed of hard Lewis acid metal ions, such as Fe3+, Al3+, and Zr4+, have good stability. These highly charged ions can generate strong electrostatic adsorption between organic ligands and resist erosion from H2O and acidic or basic reactants.

3.2. Effects on Rice Yield and Biomass

Several studies have demonstrated that foliar spraying with Fe-based materials reduces heavy metal stress in plants, increases iron uptake, and increases rice biomass and yield [40,41,42]. As shown in Figure 2a, the rice grain yield of the S1 group was 6806.6 kg/ha. In comparison, the yields of the S3 and S4 groups were significantly greater, with increases of 19.82% and 19.86%, respectively. These results were consistent with those of a previous study [14,43]. The grain yield was slightly affected by the S2 treatment; however, treatment with agents that contain organic matter significantly increased the grain yield, likely due to the promotion of Fe uptake by plant-derived HA. The nutrient release rate and pattern of MIL-88@SA were associated with crop growth and increased rice yield. The wet weight of the aboveground rice parts harvested after the various treatments ranged from 45 to 52 g/plant, similar to that of the S1 group (p > 0.05). The rice parameters (e.g., leaf length, plant height, and number of tillers) barely increased (Figure 2b and Figure S4), indicating that foliar spraying of MIL-88@SA did not adversely affect rice biomass. Moreover, considering the potential environmental risks, the selection of Fe-based MOFs was made with safety considerations. Fe is a major element in the Earth’s crust and an essential micronutrient for both plants and humans, and its use at appropriate levels poses minimal ecological risk. Therefore, the application of MIL-88@SA is unlikely to have harmful effects on the environment or rice growth, further supporting its suitability as a safe foliar passivation agent. Soil contaminated with As and Cd affects plant growth by reducing photosynthesis and decreasing mineral nutrient uptake. The SPAD value represents the chlorophyll-metabolizing capacity, with a relatively high SPAD index within a certain range indicating a relatively high heavy metal detoxification capacity [44]. As shown in Figure 2d, the SPAD values of the S1 group at the tillering and flowering stages were relatively low, whereas those of the S4 group increased (p < 0.05) by 32.3% and 34.9%, respectively. The lower SPAD values of the rice plants with no treatment may have resulted from As and Cd toxicity. Fe is a cofactor of antioxidant enzymes that protects plants from As and Cd stress by increasing chlorophyll synthesis [45,46,47]. The continuous supply of Fe to the S4 group increased photosynthesis during As and Cd stress, enhancing the rice plants’ tolerance of these contaminants.
As shown in Figure 3, the contact angles on the underside of the rice leaf for water (a), MIL-88 (b), and MIL-88@SA (c) were 123.2°, 132.6°, and 106.8°, respectively. The SA coating significantly reduces the contact angle of MIL-88 because of the hydrophilic hydroxyl and carboxyl groups in SA, improving the adhesion and utilization efficiency. Previous studies reported water contact angles between 140.08° and 146.25° for rice leaves and between 130.79° and 134.77° for pectin-coated Fe-MOF. The lower angle (106.8°) of MIL-88@SA resulted in enhanced wettability, which reduced loss from runoff and aided nanoparticle penetration via stomata. Figure 3e shows that MIL-88@SA particles partially collapse from their spindle shape into small irregular clusters near the stomata and trichomes, which enables them to embed into the leaf surface and enter through stomata. The rough, hydroxyl/carboxyl-rich surfaces of the trichomes adsorb MIL-88@SA via hydrogen bonds or electrostatic forces, creating “physical anchors” that promote local accumulation [48]. Epidermal secretions and moist zones near stomata further enhance adhesion between the hydrophilic SA shell and the leaf surface.

3.3. Distribution of As and Cd in Different Tissues of Rice Plants

The effects of various treatments on the As and Cd contents in rice tissues are shown in Figure 4. The Cd content in the S1 group was 0.26 ± 0.03 mg/kg in the grain at harvest, which exceeded the national rice standard threshold of 0.2 mg/kg. The content of organic arsenic in the rice tissues accounted for less than 1% of the total arsenic. Thus, the effects of the foliar inhibitors on organic arsenic can be largely disregarded [49]. The inorganic arsenic content in the grains was 0.19 ± 0.01 mg/kg, which represents a potential health risk. Compared with the S1 group, the S2, S3, and S4 groups had reduced grain Cd contents of 0.13 ± 0.03 mg/kg, 0.13 ± 0.05 mg/kg, and 0.08 ± 0.01 mg/kg, with decreases of 48.5%, 49.4%, and 67.8%, respectively. Moreover, the iAs content was reduced to 0.15 ± 0.02 mg/kg, 0.14 ± 0.02 mg/kg, and 0.15 ± 0.01 mg/kg in the S2, S3, and S4 groups, with decreases of 20.1%, 25.7% and 22.8%, respectively. In our study, the S2 and S3 groups were sprayed twice at the tillering and flowering stages, whereas the S4 group was sprayed only once at the tillering stage. Therefore, MIL-88@SA effectively mitigated As and Cd accumulation in rice grains.
Several studies have indicated that the formation of iron plaques reduces the mobility of Cd through adsorption or coprecipitation [50,51]. However, the Cd concentration in the roots of the rice plants in the S3 and S4 groups was greater than that in the S1 group. Similar results were observed after the application of nano-Fe3O4-modified biochar [52]. The basis for these results was as follows: (i) the increased content of Fe promoted the deposition of large amounts of Cd on the surface of rice roots, where it was converted into a source of Cd; (ii) Cd was transported into the roots by iron transporters. Both the S2 and S4 groups had decreased As content in the roots, whereas the S3 group showed the opposite trend. These results indicated that iron plaque induced by Fe-based foliar inhibitors had a limited effect on As and Cd uptake by the roots. This promoted As and Cd transport to the rice roots and increased As and Cd sequestration by the roots, thereby reducing As and Cd uptake in the aboveground parts of the rice plants. The Cd content in the stems decreased from 0.25 ± 0.04 mg/kg to 0.12–0.13 mg/kg following foliar application. Interestingly, the leaf Cd content significantly increased from 0.11 ± 0.05 mg/kg in the S1 group to 0.33 ± 0.03 mg/kg in the S4 group. Furthermore, the Fe content increased by 90.1%, 133.7%, and 215.6%, respectively (Table S2). These results suggested that Fe had a positive effect on immobilizing Cd in the leaves. A similar phenomenon was observed following the foliar application of DMSA and ZIF-8@Ge [53,54]. Foliar spraying of Fe did not affect the As levels in the leaves or stems. In the S3 group, the As content in the stems increased by 194.3%. FeCl3 + HA treatment may regulate the availability and mobility of As, likely due to the complexation of HA with As and Fe in the stems [55]. Pan et al. [56] reported that foliar application of silica NPs significantly increased the content of As in the nodes and inhibited the migration of As to leaves and grains.

3.4. Correlation Analysis of Elements in Rice Tissue

Mineral elements often interact with each other because they have analogous chemical properties and interrelated metabolic pathways [57]. Thus, foliar application of Fe to rice may effectively decrease the As and Cd contents in the grains [58]. The Fe, Ce, As, Pb, and Cd levels presented similarities and significant correlations (Figure S5). Several studies have demonstrated that rare earth elements improve plant absorption and heavy metal accumulation [59,60]. However, Zhang et al. [61] reported that 100 mg/kg CeO2 NPs increased the Fe, Zn, and Mn micronutrient contents in rice shoots but had no effect on the accumulation of As and Cd. Therefore, the effect of Ce was not considered in this study. As shown in Figure 5, Fe was significantly positively correlated with As in the stems and significantly positively correlated with Cd in the leaves (p < 0.05). Fe in the grains was negatively correlated with As and Cd (p < 0.05), which indicated that As and Cd/Fe may use similar transporters in rice plants and exhibit antagonistic interactions. Shaibur, Sera et al. [62] reported that As decreased Fe translocation in rice xylem. He et al. [63] reported that Fe prevented Cd uptake by competition and by inhibiting IRT1 expression. Although there are no known multi-element transporters, the interactions among Cd, As, and other elements may be elucidated using ion omics. The Cd accumulated in old leaves is transported to rice grains through the phloem vascular system in the same manner as photosynthesis [64]. In the present study, Cd in the leaves and grains was significantly negatively correlated (Figure S6). This result indicated that foliar application of Fe mitigated the transfer of Cd from the leaves to the grains and reduced the Cd content in the grains.

3.5. Mechanisms by Which Foliar Inhibitors Mitigate As and Cd Accumulation in Rice

The xylem is the main pathway for the distribution of essential/nonessential nutrients absorbed by roots to aboveground tissues. Like many plants, in which salt stress accelerates the development of the root endodermis and exodermis, xylem thickening induced by heavy metal stress plays an important role in reducing the uptake and translocation of heavy metals [65,66]. With sufficient resolution, CLSM can reveal variations in the xylem within different tissues. Compared with those in the S1 group, no significant changes in the xylem thickness of the rice roots, stems, or leaves were observed in the S4 group (Figure S7). In addition, the dry-to-fresh weight ratio and other physiological indices of the aboveground rice plants did not notably vary (Figure 2). These results were probably due to uncontrollable factors, such as temperature, humidity, and other field conditions. This finding also indicated that dilution of the heavy metals did not affect the rice growth. In contrast, the positive effect of MIL-88@SA significantly alleviated the accumulation of As and Cd in the rice grains.

3.5.1. Mechanisms of As Mitigation in Rice Plants

Applying Fe to the soil decreases the accumulation of As in rice tissues by increasing the adsorption capacity of Fe oxides for As [65]. However, the application of Fe to the soil tends to convert it to insoluble forms, rendering it ineffective. Thus, the strategy of foliar spraying of Fe has gradually gained increasing attention. Notably, few studies have explored the effects of foliar Fe or Si application on total As accumulation in rice plants, especially inorganic As in rice grains [17]. In this study, we discovered that various Fe treatments effectively reduced the inorganic As content in rice grains, whereas the actual blocking effect on As under field conditions was insignificant. Changes in the As content in the stems and leaves were not detected in response to the various spraying treatments, whereas a positive correlation between Fe and As was observed in the stems (Figure 5b). In the S3 group, the levels of both Fe and As in the stems increased. In the presence of Fe, dissolved organic matter (DOM) may bind substantial amounts of As by forming As–Fe–DOM complexes [66,67]. A study on the use of nanoscale colloidal silica as a foliar inhibitor similarly reported that As accumulation in rice plants was reduced by enhancing the co-localization of Si and As in the stem cell wall [68,69]. In addition, during As uptake by rice, iron plaque can adsorb, shield, or buffer As in the soil [69]. We observed a significant reduction in As content in the roots of the S4 group (Figure 4a). The reductive dissolution of iron oxide in the iron plaque under flooding conditions may lead to the formation of highly insoluble Fe3(AsO4)2, thereby preventing As uptake by the roots. Moreover, calculations revealed that AsTF (TFRoot–stem) significantly increased in the S2 and S3 groups and that AsTF (TFStem–leaf) significantly increased by 59.1% in the S4 group (Figure 6b). These results were consistent with the proposed mechanisms for mitigating iAs accumulation in grains. In addition, the SPAD index of the rice leaves in the S4 group significantly increased, which enhanced the As detoxification ability to some extent (Figure 2d). Previous studies reported that foliar application of Si or Se mitigated the phytotoxicity of As by enhancing the antioxidant capacity and photosynthesis of rice [70]. These findings indicate that foliar spraying of Fe may alleviate the accumulation of As in rice. More in-depth studies are needed to elucidate the underlying mechanism.
In addition to these physiological and biochemical mechanisms, the antagonistic interaction between Fe and As may be mediated by specific root channel proteins involved in ion transport. Amos Musyoki Mawia et al. [71] reported that As (III), the predominant inorganic form of As under flooded paddy soil conditions, is primarily taken up by rice roots through aquaporin channels such as OsLsi1, which also mediate the uptake of silicic acid. When present at sufficient concentrations, Fe may interfere with the function or expression of these channels either directly or indirectly, thereby limiting the entry of As into the root system [72]. Moreover, Fe3+ may induce oxidative stress or alter membrane permeability, further modulating transporter activity. Recent studies suggest that excess Fe may downregulate OsLsi1 or OsLsi2, reducing the transport efficiency of As across the root cortex and into the xylem [73]. Collectively, these results underscore the complex antagonistic relationship between Fe and As in rice roots, which is likely to involve both physicochemical barriers and the modulation of membrane transport proteins. Although foliar Fe application had limited efficacy in reducing As translocation under field conditions, its capacity to alter As uptake dynamics at the root level warrants further investigation.

3.5.2. Mechanisms of Cd Mitigation in Rice Plants

Owing to their similar chemical properties and plant transport pathways, Fe ions play a key role in regulating the uptake of Cd in rice [74,75]. In the present study, Cd accumulation in rice grains was significantly decreased in the S4 group (Figure 4a). The formation of iron plaques on the surface of rice roots may decrease the Cd content in the roots by immobilizing and sequestering Cd; however, several studies, including ours, have yielded contradictory results [76,77]. Compared with those in the S1 group, the concentrations of Fe and Cd in the roots in the S3 and S4 groups significantly increased (Table S2). These findings indicated that the Fe-based foliar inhibitors promoted the development of iron plaques, which adsorb Cd and serve as a source of Cd for the roots. The role of Fe/Mn plaques as barriers or substrates for the storage of Cd is controversial [78]. Therefore, the exact role of root Fe/Mn plaques under various Fe conditions requires further study. This effect may depend on competing ion interactions, pH, and other factors [79]. After the various spraying treatments, the Fe and Cd concentrations in the leaves were positively correlated (Figure 5c). The Fe and Cd contents significantly increased, particularly in the S4 group. In addition, foliar application of Fe significantly increased the CdTF (TFStem–leaf) from 184.8% to 354.3%. In contrast, the CdTF (TFLeaf–grains) in the S1 group significantly decreased from 3.19 ± 0.59 between 0.25 and 0.57 (Figure 7). The foliar application of Fe altered the redistribution of Cd in the rice plants, with Fe exerting a positive effect on immobilizing Cd in the leaves. LA–ICP–MS is an excellent tool for in situ analysis of the spatial elemental distribution in plant tissues, enabling accurate distinction of the current locations of heavy metals [80]. Elemental mapping analysis of untreated leaves revealed a small amount of Cd in the leaves, whereas in the S4 group after spraying, Cd was primarily concentrated in the vascular bundles of the main leaf veins and chloroplasts at concentrations ranging from 2 to 4 mg/kg. Moreover, the content and signal of Cd are notably lower in the epidermis than in leaf mesophyll cells [81]. Although Fe was distributed throughout the leaves, it presented a spatial distribution pattern similar to that of Cd in the main leaf veins, with a relatively high content at locations enriched with Cd (Figure 8b). Because of their similar chemical properties, Fe and Cd exhibit an overlapping spatial distribution pattern [82,83]. The cell wall and its components act as a primary barrier against metal ions, particularly negatively charged low-methoxy pectin, which has a high Fe-binding capacity. Thus, Cd deposition in the cell wall is an important mechanism for Cd tolerance in rice [20,84]. Zhang, et al. [76] reported that various Fe treatments increased the levels of ionic soluble pectin, which providing more Cd binding sites in the root cell wall. Cd increased Fe accumulation in Arabidopsis by enhancing cell wall polysaccharides [85].
These results indicate that increased Fe content in leaves may increase cell wall integrity and promote the coaccumulation of Fe and Cd through electrostatic interactions within the mesophyll cell wall. Additionally, oxygen atoms on the surface of Fe3O4 can form stable complexes with Cd2+, thereby reducing Cd mobility and toxicity [86]. Oxygen-containing functional groups such as –COOH, –O–, and Fe–O on the surface of MIL-88@SA may facilitate the formation of Fe–O–Cd complexes, effectively immobilizing Cd in leaf tissues. Previous studies have reported antagonistic interactions between Fe and Cd in plant tissues. For example, Wang et al. [14,41] found a negative correlation between the Fe and Cd concentrations in leaves under different Fe treatments. Adequate foliar Fe supply has been shown to reduce root Fe uptake and limit Cd transport from the roots to aerial parts. Similarly, in the present study, foliar application of Fe-HA led to reduced Cd accumulation in rice grains. Overall, foliar spraying of Fe inhibited Cd translocation to the grain by promoting its retention in the roots and leaves. MIL-88@SA treatment significantly influenced Cd distribution in rice tissues and enhanced Cd immobilization in leaves, thereby reducing its entry into the edible portions of the plant.

4. Conclusions

An Fe-based foliar inhibitor, MIL-88@SA, was synthesized via a two-step method, forming a metastable state between the solution and solid particles. Compared with conventional Fe-based solutions and nanoparticles, MIL-88@SA offers a novel strategy for mitigating As and Cd accumulation in rice paddies. Field trials demonstrated its efficacy, with a 19.82% increase in rice yield and a 22.8% reduction in iAs and a 67.8% reduction in Cd in the grains. The mitigation mechanisms involve sustained Fe release, which enhances stress tolerance and internal redistribution of As and Cd, which limits their translocation to grains. Fe facilitates Cd sequestration in leaves while reducing its accumulation in edible parts. These findings highlight MIL-88@SA as a promising candidate for dual As-Cd mitigation and advance the application of MOFs in sustainable rice production.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy15071710/s1, Text S1. Analysis of the trace element content. Text S2. Preparation of using LSCM and LA-ICP-MS. Figure S1. Location of the study site. Figure S2. The standard calibration of the target elements by LA-ICP-MS. Figure S3. (a) TEM images of MIL-88, (b) Survey XPS of MIL-88@SA O1s, (c) Survey XPS of MIL-88@SA, and (d) Thermal stability of MIL-88@SA. Figure S4. (a) the leaf length, (b) the tiller number of rice plants at harvest stage. Bars followed with the different letter indicate there is statistically significant difference, while the same letter indicate there is no statistically significant difference (p < 0.05; ANOVA-Duncan test). Figure S5. The (a) gravel map, and (b) cluster analysis of all elements. Figure S6. The correlation of target elements in the different tissues at the harvest stage. Figure S7. Confocal microscopy images of typical suberin patterns in the main roots, stems, and leaves under spraying CK and MIL-88@SA. Table S1. LA-ICP-MS parameters. Table S2. The concentration of As, Cd, and Fe in different tissues at the harvest by different treatments.

Author Contributions

S.W. provided ideas and designed the research study. T.W., L.L. (Lei Li) and Z.J. performed sample pretreatment and data analysis. T.W., W.L., H.C. and L.L. (Lidan Lei) wrote and polished the manuscript. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (42177012), the Natural Science Foundation Project of Chongqing, China (CSTB2022NSCQ-MSX1453), and the Open Project of Sichuan University Key Laboratory of Optimization and Application of Functional Molecular Structure (NO. GNFZ202408).

Data Availability Statement

The data presented in this study are available on request from the corresponding author. The data originate from our research group’s proprietary project and are subject to intellectual property protection; therefore, access to raw data requires explicit permission from the corresponding author.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

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Figure 1. TEM images of MIL-88 and MIL-88@SA (a,b); XRD patterns of MIL-88 and MIL-88@SA (c); FT-IR spectra of MIL-88 and MIL-88@SA (d); XPS spectra of MIL-88 and MIL-88@SA (e,f); survey scan and C 1s region (e), Fe 2p region (f).
Figure 1. TEM images of MIL-88 and MIL-88@SA (a,b); XRD patterns of MIL-88 and MIL-88@SA (c); FT-IR spectra of MIL-88 and MIL-88@SA (d); XPS spectra of MIL-88 and MIL-88@SA (e,f); survey scan and C 1s region (e), Fe 2p region (f).
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Figure 2. (a) The biomass of rice plants, (b) height at the harvest stage, (c) weight ratio of rice plants at the harvest stage, and (d) SPAD values at the tillering, flowering, and harvesting stages. Bars followed by different letters are significantly different, whereas those with the same letter are not significantly different (p < 0.05; ANOVA–Duncan test).
Figure 2. (a) The biomass of rice plants, (b) height at the harvest stage, (c) weight ratio of rice plants at the harvest stage, and (d) SPAD values at the tillering, flowering, and harvesting stages. Bars followed by different letters are significantly different, whereas those with the same letter are not significantly different (p < 0.05; ANOVA–Duncan test).
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Figure 3. Contact angle measurements of rice leaves treated with different foliar inhibitors: (a) water, (b) MIL-88, (c) MIL-88@SA, (d) control leaf surface (cryo-TEM), and (e,f) leaf surfaces after MIL-88@SA spraying.
Figure 3. Contact angle measurements of rice leaves treated with different foliar inhibitors: (a) water, (b) MIL-88, (c) MIL-88@SA, (d) control leaf surface (cryo-TEM), and (e,f) leaf surfaces after MIL-88@SA spraying.
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Figure 4. (a) Cd and (b) As concentrations in different rice tissues after foliar application of S1–S4. Different letters indicate significant differences between each treatment according to Duncan’s test (p < 0.05).
Figure 4. (a) Cd and (b) As concentrations in different rice tissues after foliar application of S1–S4. Different letters indicate significant differences between each treatment according to Duncan’s test (p < 0.05).
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Figure 5. Correlation analysis of relevant elements in (a) roots, (b) stems, (c) leaves, and (d) grains.
Figure 5. Correlation analysis of relevant elements in (a) roots, (b) stems, (c) leaves, and (d) grains.
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Figure 6. (a) Translocation factors of As from roots to stems, (b) from stems to leaves, (c) from leaves to grains, and (d) from stems to grains at harvest. The error bars represent the standard deviations of factors from three replicate datasets.
Figure 6. (a) Translocation factors of As from roots to stems, (b) from stems to leaves, (c) from leaves to grains, and (d) from stems to grains at harvest. The error bars represent the standard deviations of factors from three replicate datasets.
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Figure 7. (a) Translocation factors of Cd from roots to stems, (b) from stems to leaves, (c) from leaves to grains, and (d) from stems to grains at harvest. The error bars represent the standard deviations of factors from three replicate datasets.
Figure 7. (a) Translocation factors of Cd from roots to stems, (b) from stems to leaves, (c) from leaves to grains, and (d) from stems to grains at harvest. The error bars represent the standard deviations of factors from three replicate datasets.
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Figure 8. LA–ICP–MS images of the 75As, 111Cd, and 57Fe distribution maps at the leaf freezing microtome cross sections sampled 10 cm from the node. The image distribution maps of 75As,111Cd, and 57Fe in the leaves of (a) CK and (b) MIL-88@SA. The 13C signal was used to normalize the elemental signal intensities. The target elemental concentrations are shown as heatmaps, where rad represents the highest intensities, dark blue represents the weakest intensities. The dosage unit of the heatmaps is mg/kg.
Figure 8. LA–ICP–MS images of the 75As, 111Cd, and 57Fe distribution maps at the leaf freezing microtome cross sections sampled 10 cm from the node. The image distribution maps of 75As,111Cd, and 57Fe in the leaves of (a) CK and (b) MIL-88@SA. The 13C signal was used to normalize the elemental signal intensities. The target elemental concentrations are shown as heatmaps, where rad represents the highest intensities, dark blue represents the weakest intensities. The dosage unit of the heatmaps is mg/kg.
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Table 1. Basic physiochemical properties of the soil.
Table 1. Basic physiochemical properties of the soil.
Paddy PropertiesValue
Total Cd, mg·kg−10.72 ± 0.078
Total As, mg·kg−118.24 ± 1.625
DTPA-extractable As, mg·kg−14.93 ± 0.786
DTPA-extractable Cd, mg·kg−10.55 ± 0.070
pH6.02 ± 0.637
Soil organic matter, %2.26 ± 0.482
Total nitrogen, g·kg−12.64 ± 0.123
Total phosphorus, g·kg−10.37 ± 0.040
Available K, mg·kg−1132.33 ± 1.528
Cation exchange capacity (CEC), cmol·kg−15.71 ± 0.051
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Wang, T.; Cui, H.; Li, W.; Jiang, Z.; Li, L.; Lei, L.; Wei, S. The Mechanism of an Fe-Based MOF Material as a Foliar Inhibitor and Its Co-Mitigation Effects on Arsenic and Cadmium Accumulation in Rice Grains. Agronomy 2025, 15, 1710. https://doi.org/10.3390/agronomy15071710

AMA Style

Wang T, Cui H, Li W, Jiang Z, Li L, Lei L, Wei S. The Mechanism of an Fe-Based MOF Material as a Foliar Inhibitor and Its Co-Mitigation Effects on Arsenic and Cadmium Accumulation in Rice Grains. Agronomy. 2025; 15(7):1710. https://doi.org/10.3390/agronomy15071710

Chicago/Turabian Style

Wang, Tianyu, Hao Cui, Weijie Li, Zhenmao Jiang, Lei Li, Lidan Lei, and Shiqiang Wei. 2025. "The Mechanism of an Fe-Based MOF Material as a Foliar Inhibitor and Its Co-Mitigation Effects on Arsenic and Cadmium Accumulation in Rice Grains" Agronomy 15, no. 7: 1710. https://doi.org/10.3390/agronomy15071710

APA Style

Wang, T., Cui, H., Li, W., Jiang, Z., Li, L., Lei, L., & Wei, S. (2025). The Mechanism of an Fe-Based MOF Material as a Foliar Inhibitor and Its Co-Mitigation Effects on Arsenic and Cadmium Accumulation in Rice Grains. Agronomy, 15(7), 1710. https://doi.org/10.3390/agronomy15071710

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