Next Article in Journal
Densification of Genetic Map and Stable Quantitative Trait Locus Analysis for Amino Acid Content of Seed in Soybean (Glycine max L.)
Previous Article in Journal
Predicting the Threat Status of Mosses Using Functional Traits
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 13
Issue 15
10.3390/plants13152018
plants-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

Comparing the Effects of Lime Soil and Yellow Soil on Cadmium Accumulation in Rice during Grain-Filling and Maturation Periods

by
Hu Wang
1,2,
Lang Teng
1,
Xu Mao
1,
Tengbing He
1 and
Tianling Fu
1,2,*
1
Institute of New Rural Development, Guizhou University, Guiyang 550025, China
2
Guizhou Chuyang Ecological Environmental Protection Technology Co., Ltd., Guiyang 550025, China
*
Author to whom correspondence should be addressed.
Plants 2024, 13(15), 2018; https://doi.org/10.3390/plants13152018
Submission received: 19 June 2024 / Revised: 12 July 2024 / Accepted: 16 July 2024 / Published: 23 July 2024
(This article belongs to the Special Issue Soil Heavy Metal Pollution and Agricultural Product Quality)
Browse Figures
Versions Notes

Abstract

:
The karst area has become a high-risk area for Cadmium (Cd) exposure. Interestingly, the high levels of Cd in soils do not result in an excessive bioaccumulation of Cd in rice. Carbonate rock dissolution ions (CRIs) could limit the accumulation and translocation of Cd in rice. CRIs can become a major bottleneck in the remediation and management of farmlands in karst areas. However, there is limited research on the effects of CRIs in soils on Cd accumulation in rice. The karst area of lime soil (LS) and the non-karst areas of yellow soil (YS) were collected, and an external Cd was added to conduct rice cultivation experiments. Cd and CRIs (Ca2+, Mg2+, CO32−/HCO3−, and OH−) in the rice–soil system were investigated from the grain-filling to maturity periods. The results showed that CRIs of LS were significantly higher than that of YS in different treatments. CRIs of LS were 2.05 mg·kg−1 for Ca2+, 0.90 mg·kg−1 for Mg2+, and 42.29 mg·kg−1 for CO32− in LS. CRIs could influence DTPA Cd, resulting in DTPA Cd of LS being lower than that of YS. DTPA Cd of YS was one to three times larger than that of YS. Cd content in different parts of rice in YS was higher than that of LS. Cd in rice grains of YS was one to six times larger than that of LS. The uptake of Cd from the soil during Filling III was critical in determining rice Cd accumulation. CRIs in the soil could affect Cd accumulation in rice. Ca2+ and Mg2+ had significant negative effects on Cd accumulation of rice at maturity and filling, respectively. CO32−/HCO3− and OH− had significant negative effects on DTPA Cd in soil.

1. Introduction

Soil pollution by heavy metals has been both serious and widespread, which has become an unstable factor that affects crop production and food safety [1]. For example, the mean concentration of Cd in rice of Hunan (0.49 mg/kg), Guangdong (0.42 mg/kg), Guizhou (0.33 mg/kg), and Jiangxi (0.3 mg/kg) were higher than the food safety screening values (0.2 mg/kg) (GB 2762–2022) in China [2]. Among various heavy metals, Cd is of particular concern because of its high mobility, high toxicity, easy accumulation, and difficulty in elimination [3,4]. The National Soil Pollution Survey Bulletin issued by the Chinese government in 2014 indicated that the farmland soil pollutants at 19.4% of points exceeded the standard, Cd in 7.0% of the points exceeded the standard rate [5], and Cd was concentrated in the southwestern karst region (e.g., Guizhou, Guangxi, Chongqing). In China, it is also estimated that approximately 10 million hm−2 of contaminated farmland and 3.33 million hm−2 of farmlands are unsuited for farming due to pollution [2]. The enrichment of Cd in the soil is usually also derived from the parent rock [6]. Previous studies have shown that the soil Cd in carbonate, clasolite, and quaternary sediment regions exceeded the risk screening values of 70.77%, 6.89%, and 18.75%, respectively, in Guangxi, among which the carbonate rock region exceeded the limit most seriously [7]. However, the rice Cd exceeded the national standard in carbonate, clasolite, and quaternary sediment regions were 2%, 13.79%, and 9.38%, respectively [7]. Soil derived from carbonate rocks has higher total Cd and lower mobile Cd proportion than soil from the non-karst areas (clasolite and quaternary sediment regions), which had little impact on the quality risk of crops [7,8,9]. Similarly, the high levels of Cd in potato-/rice-planting soils would not result in an excessive bioaccumulation of Cd in Guizhou [9,10]. Therefore, Cd concentration in crops was lower in karst areas with a high Cd background (0.65 mg·kg−1).
There is a prominent issue of soil Cd exceeding the standard in the karst region in China. The standards of soil Cd were 0.3 (pH ≤ 5.5), 0.4 (5.5 < pH ≤ 6.5), 0.6 (6.5 < pH ≤ 7.5), and 0.6 (pH > 7.5) mg·kg−1 based on soil environmental quality risk control standards for soil contamination of agricultural land (GB 15618–2018) in China [9]. However, the soil Cd activity in this region is low, and rice exceeding the national standard is much lower than that in non-karst areas [6,7,9,11,12,13]. Pu et al. [14] and Fang et al. [15] found that most soil samples in the karst region were rich in CRIs. It was demonstrated that Cd2+ in the soil can form CdCO3 precipitation, Cd(OH)2 precipitation, and (Cd, Ca)CO3 coprecipitation with Ca2+, CO32−, and OH− under alkaline conditions, reducing the activity of Cd in the soil [16,17,18]. Moreover, Ca2+, Mg2+, and Cd2+ have the same positive charge and specific surface area and can compete with Cd for plant uptake. Ca and Mg are among the 17 essential nutrients for plant growth [19]. They are active in plants and inhibit Cd migration in plants [20,21]. The supplementation of both Ca and Mg decreased Cd accumulation and translocation in rice tissues in Cd-polluted soil [8]. It is inferred that the typical carbonate erosion in the karst region forms the rich components of CRIs, which plays an important role in regulating the migration, absorption, and trans-shipment of Cd in the soil–water–crop system.
The karst area has become a high-risk area for Cd exposure [9]. In recent years, several methods have been studied to control Cd risks in karst areas, such as water management, fertilization, physical treatments, chemical remediation via the addition of soil amendments, bioremediation, and phytoremediation [8]. Moreover, a large number of pilot demonstration projects to treat and restore contaminated soil were launched. However, soil derived from carbonate rocks has higher total Cd and lower mobile Cd proportion [7]. Li et al. [7] found that soil carbonates raised soil pH of Cd, significantly reducing the bioavailability of Cd in karst areas. The classification of agricultural land environmental quality and agricultural land safe usage based on Cd content in the soil has a wide deviation. CRIs can become a major bottleneck in the remediation and management of farmlands in karst areas, thus resulting in immeasurable ecological risk and waste of cultivated land resources.
In this study, the karst area of LS and the non-karst areas of YS were collected, and an external Cd was added to conduct rice cultivation experiments. The primary aims of this work were to (1) analyze the effects of dynamic change in CRI content in the root-zone soil on Cd accumulation in rice during grain-filling and maturation Periods; (2) explore the inhibitory effects of CRIs in the soil on Cd accumulation during the rice filling–ripening period. However, there is limited research on the effects of CRIs in soils on Cd accumulation in rice. The results of this study will provide a theoretical basis for the safe utilization of Cd-contaminated soils in karst areas and safe rice production.

2. Materials and Methods

2.1. Plant Materials and Experimental Design

The experiment used soil samples collected from Huaxi District, Guizhou Province. LS was derived from dolomite rocks. YS was derived from mudstone rocks. LS and YS were collected from a surface (0–20 cm) of farmland soil. The basic physical and chemical properties of YS and LS are shown in Table 1. The collected soil was transported to a laboratory for natural air drying, and large gravel, stone, and branches were removed. The soil was ground through a 2 mm sieve and mixed thoroughly for later use.
In 2022, a rice pot experiment was conducted at the Guiyang Comprehensive Test Station of the Guizhou Academy of Agricultural Sciences, Guizhou, China. Each pot (15 cm × 20 cm) was filled with 20 kg air-dried YS and LS, respectively. An external CdCl2 was added in LS and YS to conduct rice cultivation experiments. CdCl2 treatments in YS/LS were designed as 0.72, 1.65, 3.25, and 4.20 mg·kg−1, regarded as YS1/LS1, YS2/LS2, YS3/LS3, and YS4/LS4, respectively. Each treatment was repeated three replicates. The pot experiment was completely randomized with three replicates and a total of 24 pots. The soil had a balance period of 60 d. Base fertilizers were applied and thoroughly mixed with soil, filled with water until they reached saturation, and allowed to equilibrate for 7 d. The base fertilizer used was (NH4)3PO4, with a phosphorus pentoxide content of 210 mg·kg−1, urea with a nitrogen content of 280 mg·kg−1, and K2CO3 with a K2O content of 200 mg·kg−1. Rice was planted. The rice cultivar, C Liangyouhuazhan, was obtained from the Rice Research Institute, Guizhou Academy of Agricultural Sciences. During the tillering stage, 5 g/pot (equivalent to 41.7 kg·hm−2) of urea (N ≥ 46.2%) was applied as topdressing. During the early filling stage, 5 g/pot (equivalent to 41.7 kg·hm−2) of compound fertilizer (N:P:K = 16:8:18) was applied as topdressing.

2.2. Sample Collection and Preparation

Rice grain filling is the most important physiological process of grain formation, and it is also the decisive stage that determines grain weight, yield, and rice quality [22]. In this study, rice grain filling was measured at the first week of filling (Filling I), the second week of filling (Filling II), and the third week of filling (Filling III). Soil and rice plant samples were collected as follows: Filling I (6 September), Filling II (13 September), Filling III (20 September), and maturity (27 September, the maturity stage). There were the 96-soil sample and the 312-rice plant sample. Soil samples were air-dried in the laboratory and separated by using the coning and quartering method. They were then passed through a 2 mm and 0.149 mm nylon sieve for subsequent analyses. Rice plant samples were collected and transported to the laboratory. The plants were washed with tap water to remove the soil on the roots and then rinsed three times with ultrapure water. They were then separated into five parts: roots, stems, leaves, cobs, and grains. The separated parts were oven-dried at 105 °C for 2 h and then at 70 °C until reaching a constant weight. The grains were dehulled to obtain the glumes and brown rice samples, which were ground into powder using an agate mortar and sieved through a 0.425 mm nylon sieve for subsequent analyses.

2.3. Chemical Analysis and Quality Control

Soil pH was determined using a distilled water extraction (soil/water ratio of 1:2.5) by the potentiometric method. Soil total alkalinity (CO32−/HCO3−) was determined by the acid–base titration method with a 1:5 soil/water ratio. A total of 0.1 g of soil sample was added to a high-pressure airtight tank and digested for total Cd, Ca, and Mg with HF (1 mL)–HNO3 (3 mL)–HClO4 (1 mL) by the autoclave at a constant temperature in the drying oven [9]. The bioavailability of Cd (DTPA-Cd) was extracted by DTPA (extraction in 5 mM diethylenetriaminepentaacetic acid). Ca2+ and Mg2+ were extracted by ultrapure water at a solid–liquid ratio of 1:5.
The sample trace elements were determined as follows: 0.2 g of the sample was added to 5 mL of nitric acid and digested in a graphite digestion instrument at 120 °C for 2 h. The digestion was complete when no white precipitate was observed in the digestion tank. The temperature was then adjusted to 150 °C to evaporate the acid to the size of soybean grains. High-purity reagents and ultrapure water were used throughout the experiment. The analysis of soil sample and rice plant sample had two replicates.
Cd content was determined by inductively coupled plasma-optical emission spectroscopy (ICP-OES-7400, Thermo Fisher Scientific, Waltham, MA, USA). Soil Ca2+ and Mg2+ were determined by atomic absorption spectrophotometry (ICE-3500, Thermo Fisher Scientific, USA).
The quality of Cd in the soil samples was controlled using the standard soil sample (Number: GBW07405) from the National Center for Standard Materials, China. The standard soil sample was as follows: Cd 0.39–0.51 mg·kg−1. The quality of Cd, Ca, and Mg in the rice plant samples was controlled using the plant standard sample (Number: GBW10048) from the National Center for Standard Materials, China. The standard plant samples were as follows: Cd 0.086–0.098 mg·kg−1, Ca 1.60–1.72 g·kg−1, and Mg 0.50–0.56 g·kg−1. Blank reagent tests were performed, and the sample recovery rate was between 90% and 110%.

2.4. Measurement of Photosynthetic Parameters

The photosynthetic parameters of rice were measured by using a portable chlorophyll meter (SPAD-502 Plus, Minolta, Tokyo, Japan) [23]. An intact leaf from three rice plants with uniform growth conditions for each plant was selected during grain-filling and maturation periods, the SPAD value was measured at the central position six times, and the average value was taken as the SPAD value for that point.

2.5. Statistical Analyses

Data sorting was performed using Excel 2019. Normal distribution test, one-way ANOVA, and Pearson correlation analysis were conducted using SPSS 22.0. Origin 2018 software was used for plotting.

3. Results

3.1. DTPA Cd Content in the Soil during Rice Filling and Maturity

The DTPA Cd of YS was higher than that of LS in different treatments (Table 2), indicating that soil derived from carbonate rocks had a lower mobile Cd proportion. DTPA Cd of YS was one to three times larger than that of YS. The DTPA Cd increased with the increase in Cd treatments. The DTPA Cd of LS and YS in different treatments increased from Filling I to Filling III and decreased from Filling III to maturity and had the highest activity in Filling III. The DTPA Cd contents for LS1, LS2, LS3, and LS4 in Filling III were 0.122, 0.473, 0.686, and 1.432 mg·kg−1, respectively. The DTPA Cd contents for YS1, YS2, YS3, and YS4 in Filling III were 0.288, 0.654, 1.013, and 2.053 mg·kg−1, respectively.

3.2. Ca and Mg Content in the Soil during Rice Filling and Maturity

The total Ca and Mg content of LS and YS in different treatments gradually decreased from rice filling to maturity, and the total Ca and Mg content in LS was significantly higher than YS (Table 3). The total Ca and Mg content of LS in different treatments had no significant difference, while YS had significant difference. Compared to Filling I, the decrease degrees of total Ca content for YS1, YS2, YS3, and YS4 in Filling III were 12.56%,11.62%, 34.46%, and 28.44%, respectively. Compared to Filling I, the decrease degrees of total Mg content for YS1, YS2, YS2, and YS2 in maturity were 30.92%, 30.78%, 42.45%, and 48.28%, respectively. The total Mg content of LS was roughly 1.7 times that of YS under the same treatment. There was an abundant karst component in LS, and formed CRIs (e.g., Ca, Mg), resulting in Ca2+ and Mg2+ in LS being higher than YS (Figure 1). Compared to Filling I, the increased degrees of Ca2+ for YS1, YS2, YS3, and YS4 in Filling III were 62.73%, 39.96%, 17.43%, and 17.46%, respectively. The Mg2+ content of LS and YS in different treatments could reach the highest level in Filling II and then decrease from Filling II to maturity. The increased degree of Mg2+ for YS from Filling I to mature became larger with the increase in Cd stress concentration. Mg2+ content in LS increased from Filling I to Filling II and decreased from Filling III to maturity.

3.3. Total Alkalinity Content and pH in the Soil during Rice Filling and Maturity

The total alkalinity and pH of LS were significantly higher than that of YS in different treatments (Figure 2). Compared to Filling I, the total alkalinity of YS1, YS2, YS3, and YS4 was highest in maturity, which increased by 13.36%, 24.34%, 33.28%, and 28.95%, respectively. The total alkalinity of LS1, LS2, LS3, and LS4 reached the maximum in Filling II and the minimum in Filling III and decreased by 20.33%, 23.65%, 31.92%, and 30.31%, respectively, from Filling II to Filling III. The pH of soil increases with the increase in OH− concentration. In LS1 and LS2 for the low Cd treatment, the pH could reach the highest level in Filling III and then decrease. In LS3 and LS4 for the high Cd treatment, the pH of YS3 increased from rice filling to maturity, and the pH of LS4 decreased. The pH of LS in different treatments was relatively stable during rice filling and maturity, except for a slight decrease in LS3 during filling, indicating that Cd treatments in LS reduced the OH− concentration in Filling III.

3.4. Cd Content in Different Parts of Rice during Rice Filling and Maturity

The Cd content in different parts of rice in YS was significantly higher than that of LS (Figure 3). Cd content of different treatments was in the following order: roots > stems > leaves > grains. Cd content in different parts of rice increased with the increase in Cd treatments. The increased degree of Cd content in different parts of rice was the most obvious from Filling II to Filling III, indicating that Filling III is the key period of Cd accumulation in rice. The increased degree of Cd content in the roots slowed down from Filling III to maturity. The high levels of Cd in soils would not result in an excessive bioaccumulation of Cd in rice. The Cd content of LS was higher than that of YS in different parts of rice. Cd in rice grains of YS was one to six times larger than that of LS. Cd in rice grains of LS and YS in different treatments did not exceed the national standard (GB 2762-2017) [5]. However, Cd treatments could increase Cd in rice grains with the increase in Cd treatments, and the Cd content of LS4 and YS4 were 0.171 and 0.108 mg·kg−1, respectively.

3.5. Total Ca and Mg Content of Rice Plants in Different Treatments at Maturity

Total Ca and Mg content of rice plants in different treatments at maturity is shown in Table 4. Total Mg content in different parts of rice increased with the increase in Cd treatments. The total Mg content of rice plants in LS was significantly higher than YS. Total Ca content in root, stem, and leaves decreased with the increase in Cd treatments. Total Ca content in grain increased with the increase in Cd treatments. The total Ca content of root and leaves in LS was significantly higher than YS.

3.6. Correlation between CRI and DTPA Cd in Soil and Cd Content in Different Parts of Rice

As shown in Table 5, there was a significant negative correlation between CRI content and DTPA Cd, indicating that CRIs in soil could reduce the activity of Cd. There was a negative correlation between Ca2+ and Mg2+content in soil and Cd content in different parts of rice (Table 6). The regulatory role of Mg2+ on chlorophyll synthesis and degradation is also shown [24]. Photosynthesis of leaves was the highest at Filling III (Figure 4), indicating that Mg2+ played an important role in rice plants. The Cd content in rice stem leaves and grains had significantly negative effects on Mg2+ content in soil at Filling III, indicating that Mg2+ played an important role in inhibiting Cd in rice at Filling III, respectively.

4. Discussion

Soil derived from carbonate rocks (e.g., dolomite, limestone) is rich in CRIs (e.g., Ca2+, Mg2+, OH−, and HCO3−) in the karst region [14,25,26]. The CRIs of YS were 0.55 mg·kg−1 for Ca2+, 0.43 mg·kg−1 for Mg2+, and 10.76 mg·kg−1 for CO32− in Guizhou (Table 1). CRIs of LS were significantly higher than that of YS in different treatments in this study (Table 1). However, our carbonate rock dissolution experiment is the first time to demonstrate that the varying soil CRIs, more importantly CRIs in LS during grain-filling and maturation periods, can reduce Cd accumulation in rice (Figure 3).
DTPA Cd of the karst area was higher than that of the non-karst areas in different treatments (Table 2). These results were the same as those observed by Li and Wei and indicated that soil derived from carbonate rocks had lower mobile Cd proportion [27,28]. However, many studies had only focused on pH playing an important role in decreasing DTPA Cd [29], ignoring the effect of CRIs. In this study, there was a negative correlation between CRI content and DTPA Cd (Table 5). Wang’s research showed that CO32−/HCO3−, and OH− can decrease DTPA Cd in soil [30]. Cd2+ can form CdCO3 precipitation, Cd(OH)2 precipitation, and (Cd, Ca)CO3 coprecipitation with Ca2+, CO32−, and OH− under alkaline conditions [17,31]. Meanwhile, CO32− can hydrolyze to generate OH−, which could form difficult-to-soluble Cd(OH)2 precipitate with Cd, thereby reducing the activity of Cd [32]. Moreover, the increase in soil pH reduces the solubility of heavy metals in the soil, increases the pH-dependent charge, and increases the adsorption of metals by soil particles [20]. HCO3− in the soil mainly affects the activity of Cd by ionization to generate CO32− and hydrolysis to generate OH−. Ca2+ and Mg2+ compete with Cd for adsorption in the soil as a plant nutrient with the same volume and valence as Cd2+ [21,33]. The classification of agricultural land environmental quality and agricultural land safe usage based on Cd content in the soil has a wide deviation, especially in karst areas [9]. CRIs played an important role in decreasing DTPA Cd in karst areas.
The Cd uptake from the soil during rice grain filling is critical for grain Cd concentrations [34]. It was found that the DTPA Cd of LS and YS in different treatments increased from Filling I to Filling III and then decreased from Filling II to maturity in this study. DTPA Cd of LS and YS in different treatments had the highest activity in Filling III. This might be related to the decrease in CO32−/HCO3−. The total alkalinity (CO32−/HCO3−) of LS1, LS2, LS3, and LS4 reached the minimum in Filling III in this study (Figure 2a). Ca2+ and Mg2+ were a component of plant cell walls and beneficial to the growth and development of plants [35,36]. As plant nutrient elements, Ca and Mg could inhibit the absorption of Cd by plants and reduce Cd toxicity in plants [8,37]. Ca2+ and Mg2+ were absorbed to inhibit the absorption of Cd, enhance the detoxification mechanism of rice, and improve its tolerance to Cd [8]. In this study, Mg2+ content in different parts of rice increased with the increase in Cd treatments (Table 4). There was a negative correlation between Ca2+ content in soil and Cd content in different parts of rice (Table 6). Ca2+ is preferentially absorbed by plants and restrained the Cd root-to-stem transport [38]. There was increased Ca2+ in different parts of rice, effectively preventing Cd transportation from roots to the stem, leaves, and grain. Ca2+ can increase the mechanical strength of cell walls, thereby fixing Cd in root cells and reducing Cd migration within the plant [39]. Ca2+ can neutralize the negative charge of the cell membrane, reducing the contact between harmful cations and the cell membrane [40].
In addition, the increased degree of Cd content in different parts of rice was the highest at Filling III. Cd content in rice grains had significantly negative effects on Mg2+ content in soil at Filling III (Table 6), indicating that Mg2+ played an important role in inhibiting Cd in rice at Filling III, respectively. Mg2+ is a necessary element for plant photosynthesis [20]. It was found that the photosynthesis of leaves was the highest at Filling III (Figure 4), which was the main source of carbohydrates in the grain and requires Mg2+ to participate in the photosynthesis process. There was an increased demand for Mg in rice, resulting in the absorption of a large amount of Mg2+ from the soil. Li found that Mg could promote plant growth in a Cd-contaminated environment, reduce the Cd concentration, and detoxify the physiological Cd toxicity in plants [8]. The Cd contents in the shoots and roots of Mg-deficient rice seedlings were higher than that of the normal-growth rice seedlings [41].
Karst areas are globally distributed and occupy about 15% of Earth’s surface [42]. There are abundant carbonate rocks in the southwestern region (e.g., Guangxi, Guizhou, and Yunnan Provinces) of China [43]. For example, Guizhou Province is the central area concentrated with exposed carbonate rocks in the southwest region, and the carbonate rock is widely distributed in an area of 130,000 km2, comprising 73% of the total area of the province [44]. There are differences between the karst area of LS and the non-karst areas of YS. There are the anomalies in the levels of high Cd in the soils of karst areas [45]. For example, the background of soil Cd is 0.659 mg·kg−1 in Guizhou, China [9]. The karst region was rich in CRIs, resulting in a lower bioaccumulation of Cd in rice. The natural phenomenon of carbonate rock dissolution in karst areas will be a strategy to treat the levels of high Cd in the soils and decrease Cd content of rice.

5. Conclusions

This study identified that the Ca2+, Mg2+, CO32−/HCO3−, and OH− of LS were significantly higher than that of YS, resulting in DTPA Cd of LS being lower than that of YS. Cd content in different parts of rice in YS was significantly higher than that of LS. The uptake of Cd from the soil during Filling III was critical in determining rice Cd accumulation. CRIs in the soil could affect Cd accumulation in rice. Ca2+ and Mg2+ had significant negative effects on Cd accumulation of rice at maturity and filling, respectively. CO32−/HCO3− and OH− had significant negative effects on DTPA Cd in soil. In future studies, molecular biology, genomics, and other methods should be used further to investigate the effects and microbial mechanisms of carbonate rock dissolution (CRD) on Cd reduction in rice.

Author Contributions

H.W.: conceptualization, methodology, data curation, writing—original draft, and writing—review and editing. L.T.: conceptualization, investigation, resources, and writing—review and editing. X.M.: investigation, methodology, and data curation. T.H.: investigation, resources, data curation, and project administration. T.F.: conceptualization, investigation, methodology, funding acquisition, and project administration. All authors have read and agreed to the published version of the manuscript.

Funding

This work was funded by the National Natural Science Foundation of China (42167003).

Data Availability Statement

Data will be made available on request.

Conflicts of Interest

Authors Hu Wang and Tianling Fu were employed by the company Guizhou Chuyang Ecological Environmental Protection Technology Co., Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

References

  1. Zhang, J.; Mu, G.; Zhang, Z.; Huang, X.; Fang, H. Speciation Variation and Bio-Activation of Soil Heavy Metals (Cd and Cr) in Rice-Rape Rotation Lands in Karst Regions. Int. J. Environ. Res. Public Health 2021, 18, 1364. [Google Scholar] [CrossRef] [PubMed]
  2. Wang, C.-C.; Zhang, Q.-C.; Yan, C.-A.; Tang, G.-Y.; Zhang, M.-Y.; Ma, L.Q.; Gu, R.-H.; Xiang, P. Heavy metal(loid)s in agriculture soils, rice, and wheat across China: Status assessment and spatiotemporal analysis. Sci. Total Environ. 2023, 882, 163361. [Google Scholar] [CrossRef] [PubMed]
  3. Godt, J.; Scheidig, F.; Grosse-Siestrup, C.; Esche, V.; Brandenburg, P.; Reich, A.; Groneberg, D.A. The toxicity of cadmium and resulting hazards for human health. J. Occup. Med. Toxicol. 2006, 1, 22. [Google Scholar] [CrossRef] [PubMed]
  4. Aziz, R.; Rafiq, M.T.; Li, T.; Liu, D.; He, Z.; Stoffella, P.J.; Sun, K.; Yang, X. Uptake of cadmium by rice grown on contaminated soils and its bioavailability/toxicity in human cell lines (Caco-2/HL-7702). J. Agric. Food Chem. 2015, 63, 3599–3608. [Google Scholar] [CrossRef] [PubMed]
  5. Huang, X.; Fan, C.; Xie, D.; Chen, H.; Zhang, S.; Chen, H.; Qin, S.; Fu, T.; He, T.; Gao, Z. Synergistic Effects of Water Management and Silicon Foliar Spraying on the Uptake and Transport Efficiency of Cadmium in Rice (Oryza sativa L.). Plants 2023, 12, 1414. [Google Scholar] [CrossRef] [PubMed]
  6. Wen, Y.; Li, W.; Yang, Z.; Zhuo, X.; Guan, D.-X.; Song, Y.; Guo, C.; Ji, J. Evaluation of various approaches to predict cadmium bioavailability to rice grown in soils with high geochemical background in the karst region, Southwestern China. Environ. Pollut. 2020, 258, 113645. [Google Scholar] [CrossRef] [PubMed]
  7. Li, C.; Yang, Z.; Yu, T.; Hou, Q.; Liu, X.; Wang, J.; Zhang, Q.; Wu, T. Study on safe usage of agricultural land in karst and non-karst areas based on soil Cd and prediction of Cd in rice: A case study of Heng County, Guangxi. Ecotoxicol. Environ. Saf. 2021, 208, 111505. [Google Scholar] [CrossRef] [PubMed]
  8. Li, X.; Teng, L.; Fu, T.; He, T.; Wu, P. Comparing the effects of calcium and magnesium ions on accumulation and translocation of cadmium in rice. Environ. Sci. Pollut. Res. 2022, 29, 41628–41639. [Google Scholar] [CrossRef] [PubMed]
  9. Wang, H.; Cai, N.; Gong, S.; Zhou, J.; He, T.; Wang, B.; Fu, T. Establishment and Optimization of Soil Cd Risk Threshold in Typical Karst Area with Potato Production, China. Bull. Environ. Contam. Toxicol. 2023, 110, 34. [Google Scholar] [CrossRef] [PubMed]
  10. Kong, X.; Liu, T.; Yu, Z.; Chen, Z.; Lei, D.; Wang, Z.; Zhang, H.; Li, Q.; Zhang, S. Heavy Metal Bioaccumulation in Rice from a High Geological Background Area in Guizhou Province, China. Int. J. Environ. Res. Public Health 2018, 15, 2281. [Google Scholar] [CrossRef]
  11. Wan, G.; Najeeb, U.; Jilani, G.; Naeem, M.S.; Zhou, W. Calcium invigorates the cadmium-stressed Brassica napus L. plants by strengthening their photosynthetic system. Environ. Sci. Pollut. Res. 2011, 18, 1478–1486. [Google Scholar] [CrossRef] [PubMed]
  12. Wen, Y.; Li, W.; Yang, Z.; Zhang, Q.; Ji, J. Enrichment and source identification of Cd and other heavy metals in soils with high geochemical background in the karst region, Southwestern China. Chemosphere 2020, 245, 125620. [Google Scholar] [CrossRef] [PubMed]
  13. Ma, H.-H.; Peng, M.; Guo, F.; Liu, F.; Tang, S.-Q.; Yang, Z.; Zhang, F.-G.; Zhou, Y.-L.; Yang, K.; Li, K.; et al. Factors Affecting the Translocation and Accumulation of Cadmium in a Soil-Crop System in a Typical Karst Area of Guangxi Province, China. Huanjing Kexue 2021, 42, 1514–1522. [Google Scholar] [CrossRef] [PubMed]
  14. Pu, J.; Yuan, D.; Xiao, Q.; Zhao, H. Hydrogeochemical characteristics in karst subterranean streams: A case history from Chongqing, China. Carbonates Evaporites 2015, 30, 307–319. [Google Scholar] [CrossRef]
  15. Guo, F.; Jiang, G.; Yuan, D. Major ions in typical subterranean rivers and their anthropogenic impacts in southwest karst areas, China. Environ. Earth Sci. 2007, 53, 533–541. [Google Scholar] [CrossRef]
  16. Ding, Y.; Luo, W.; Xu, G. Characterisation of magnesium nutrition and interaction of magnesium and potassium in rice. Ann. Appl. Biol. 2006, 149, 111–123. [Google Scholar] [CrossRef]
  17. Loganathan, P.; Vigneswaran, S.; Kandasamy, J.; Naidu, R. Cadmium Sorption and Desorption in Soils: A Review. Crit. Rev. Environ. Sci. Technol. 2012, 42, 489–533. [Google Scholar] [CrossRef]
  18. Khaliq, M.A.; James, B.; Chen, Y.H.; Saqib, H.S.A.; Li, H.H.; Jayasuriya, P.; Guo, W. Uptake, translocation, and accumulation of Cd and its interaction with mineral nutrients (Fe, Zn, Ni, Ca, Mg) in upland rice. Chemosphere 2019, 215, 916–924. [Google Scholar] [CrossRef]
  19. Sarwar, N.; Saifullah; Malhi, S.S.; Zia, M.H.; Naeem, A.; Bibi, S.; Farid, G. Role of mineral nutrition in minimizing cadmium accumulation by plants. J. Sci. Food Agric. 2010, 90, 925–937. [Google Scholar] [CrossRef]
  20. Lee, T.-M.; Lai, H.-Y.; Chen, Z.-S. Effect of chemical amendments on the concentration of cadmium and lead in long-term contaminated soils. Chemosphere 2004, 57, 1459–1471. [Google Scholar] [CrossRef]
  21. Luo, W.; Yang, S.; Khan, M.A.; Ma, J.; Xu, W.; Li, Y.; Xiang, Z.; Jin, G.; Jia, J.; Zhong, B.; et al. Mitigation of Cd accumulation in rice with water management and calcium-magnesium phosphate fertilizer in field environment. Environ. Geochem. Health 2020, 42, 3877–3886. [Google Scholar] [CrossRef] [PubMed]
  22. Huang, B.-Y.; Zhao, F.-J.; Wang, P. The relative contributions of root uptake and remobilization to the loading of Cd and As into rice grains: Implications in simultaneously controlling grain Cd and As accumulation using a segmented water management strategy. Environ. Pollut. 2022, 293, 118497. [Google Scholar] [CrossRef] [PubMed]
  23. Chen, H.; Huang, X.; Chen, H.; Zhang, S.; Fan, C.; Fu, T.; He, T.; Gao, Z. Effect of silicon spraying on rice photosynthesis and antioxidant defense system on cadmium accumulation. Sci. Rep. 2024, 14, 15265. [Google Scholar] [CrossRef] [PubMed]
  24. Gong, J.; Gao, J.; Wu, H.; Lin, L.; Yang, J.; Tang, S.; Wang, Z.; Duan, Z.; Fu, Y.; Cai, Y.; et al. Heavy metal spatial distribution, source analysis, and ecological risks in the central hilly area of Hainan Island, China: Results from a high-density soil survey. Environ. Geochem. Health 2024, 46, 210. [Google Scholar] [CrossRef] [PubMed]
  25. Gu, X.; Ma, T.; Wu, Y.; Wu, X. Hydrogeochemical Characteristics of Groundwater in the Karst Region, Southwest China. Procedia Earth Planet. Sci. 2017, 17, 245–248. [Google Scholar] [CrossRef]
  26. Geng, Y.; Pan, S.; Zhang, L.; Qiu, J.; He, K.; Gao, H.; Li, Z.; Tian, D. Phosphorus biogeochemistry regulated by carbonates in soil. Environ. Res. 2022, 214, 113894. [Google Scholar] [CrossRef] [PubMed]
  27. Li, C.; Zhang, C.; Yu, T.; Liu, X.; Xia, X.; Hou, Q.; Yang, Y.; Yang, Z.; Wang, L. Annual net input fluxes of cadmium in paddy soils in karst and non-karst areas of Guangxi, China. J. Geochem. Explor. 2022, 241, 107072. [Google Scholar] [CrossRef]
  28. Wei, X.; Bai, X.; Wen, X.; Liu, L.; Xiong, J.; Yang, C. A large and overlooked Cd source in karst areas: The migration and origin of Cd during soil formation and erosion. Sci. Total Environ. 2023, 895, 165126. [Google Scholar] [CrossRef]
  29. Hu, J.; Wu, F.; Wu, S.; Sun, X.; Lin, X.; Wong, M.H. Phytoavailability and phytovariety codetermine the bioaccumulation risk of heavy metal from soils, focusing on Cd-contaminated vegetable farms around the Pearl River Delta, China. Ecotoxicol. Environ. Saf. 2013, 91, 18–24. [Google Scholar] [CrossRef]
  30. Wang, Z.; Yi, L.; Gao, W.; Zeng, X.; Wang, Z. Impact of inorganic anions on the cadmium effective fraction in soil and its phytoavailability during salinization in alkaline soils. Sheng Tai Xue Bao 2012, 32, 7512–7518. [Google Scholar] [CrossRef]
  31. Kim, J.J.; Lee, S.S.; Fenter, P.; Myneni, S.C.B.; Nikitin, V.; Peters, C.A. Carbonate Coprecipitation for Cd and Zn Treatment and Evaluation of Heavy Metal Stability Under Acidic Conditions. Environ. Sci. Technol. 2023, 57, 3104–3113. [Google Scholar] [CrossRef] [PubMed]
  32. Zhou, Y.-M.; Long, S.-S.; Li, B.-Y.; Huang, Y.-Y.; Li, Y.-J.; Yu, J.-Y.; Du, H.-H.; Khan, S.; Lei, M. Enrichment of cadmium in rice (Oryza sativa L.) grown under different exogenous pollution sources. Environ. Sci. Pollut. Res. 2020, 27, 44249–44256. [Google Scholar] [CrossRef] [PubMed]
  33. Farzadfar, S.; Zarinkamar, F.; Modarres-Sanavy, S.A.M.; Hojati, M. Exogenously applied calcium alleviates cadmium toxicity in Matricaria chamomilla L. plants. Environ. Sci. Pollut. Res. Int. 2013, 20, 1413–1422. [Google Scholar] [CrossRef] [PubMed]
  34. Chen, H.; Wang, P.; Gu, Y.; Kretzschmar, R.; Kopittke, P.M.; Zhao, F.-J. The within-field spatial variation in rice grain Cd concentration is determined by soil redox status and pH during grain filling. Environ. Pollut. 2020, 261, 114151. [Google Scholar] [CrossRef] [PubMed]
  35. Ishfaq, M.; Wang, Y.; Yan, M.; Wang, Z.; Wu, L.; Li, C.; Li, X. Physiological Essence of Magnesium in Plants and Its Widespread Deficiency in the Farming System of China. Front. Plant Sci. 2022, 13, 802274. [Google Scholar] [CrossRef] [PubMed]
  36. Wang, T.; Chen, X.; Ju, C.; Wang, C. Calcium signaling in plant mineral nutrition: From uptake to transport. Plant Commun. 2023, 4, 100678. [Google Scholar] [CrossRef]
  37. Srivastava, R.K.; Pandey, P.; Rajpoot, R.; Rani, A.; Gautam, A.; Dubey, R.S. Exogenous application of calcium and silica alleviates cadmium toxicity by suppressing oxidative damage in rice seedlings. Protoplasma 2015, 252, 959–975. [Google Scholar] [CrossRef] [PubMed]
  38. Zhang, P.; Wei, X.; Zhang, Y.; Zhan, Q.; Bocharnikova, E.; Matichenkov, V. Silicon-Calcium Synergetic Alleviation of Cadmium Toxicity in the Paddy Soil-Rice System: From Plot Experiment to Field Demonstration. Water Air Soil Pollut. 2022, 233, 357. [Google Scholar] [CrossRef]
  39. Shi, X.; Bao, J.; Lu, X.; Ma, L.; Zhao, Y.; Lan, S.; Cao, J.; Ma, S.; Li, S. The mechanism of Ca2+ signal transduction in plants responding to abiotic stresses. Environ. Exp. Bot. 2023, 216, 105514. [Google Scholar] [CrossRef]
  40. Luo, N.; Li, Y.W.; Cai, Q.Y.; Li, H.Y.; Mo, C.H.; Wong, M.H. Cadmium in rice: Transport mechanisms, influencing factors, and minimizing measures. Environ. Pollut. 2017, 224, 622–630. [Google Scholar] [CrossRef]
  41. Chou, T.-S.; Chao, Y.-Y.; Huang, W.-D.; Hong, C.-Y.; Kao, C.H. Effect of magnesium deficiency on antioxidant status and cadmium toxicity in rice seedlings. J. Plant Physiol. 2011, 168, 1021–1030. [Google Scholar] [CrossRef]
  42. Li, S.-L.; Liu, C.-Q.; Chen, J.-A.; Wang, S.-J. Karst ecosystem and environment: Characteristics, evolution processes, and sustainable development. Agric. Ecosyst. Environ. 2021, 306, 107173. [Google Scholar] [CrossRef]
  43. Li, K.; Chen, S.; Chen, X.; Lan, X.; Huang, K. Genetic Diversity and Differentiation of Chinese Fir around Karst Landform in Guangxi. Forests 2023, 14, 340. [Google Scholar] [CrossRef]
  44. Li, S.-L.; Xu, S.; Wang, T.-J.; Yue, F.-J.; Peng, T.; Zhong, J.; Wang, L.-C.; Chen, J.-A.; Wang, S.-J.; Chen, X.; et al. Effects of agricultural activities coupled with karst structures on riverine biogeochemical cycles and environmental quality in the karst region. Agric. Ecosyst. Environ. 2020, 303, 107120. [Google Scholar] [CrossRef]
  45. Zhao, Y.; Deng, Q.; Lin, Q.; Zeng, C.; Zhong, C. Cadmium source identification in soils and high-risk regions predicted by geographical detector method. Environ. Pollut. 2020, 263, 114338. [Google Scholar] [CrossRef]
Plants 13 02018 g001
Figure 1. The Ca2+ (a) and Mg2+ (b) content of LS and YS in different treatments during rice filling and maturity.
Figure 1. The Ca2+ (a) and Mg2+ (b) content of LS and YS in different treatments during rice filling and maturity.
Plants 13 02018 g001
Plants 13 02018 g002
Figure 2. Total alkalinity content (a) and pH (b) of LS and YS in different treatments during rice filling and maturity.
Figure 2. Total alkalinity content (a) and pH (b) of LS and YS in different treatments during rice filling and maturity.
Plants 13 02018 g002
Plants 13 02018 g003
Figure 3. Cd content in root (a), stem (b), leaves (c), and grain (d) during rice filling and maturity.
Figure 3. Cd content in root (a), stem (b), leaves (c), and grain (d) during rice filling and maturity.
Plants 13 02018 g003
Plants 13 02018 g004
Figure 4. The chlorophyll content in leaves from LS (a) and YS (b) during rice filling and maturity.
Figure 4. The chlorophyll content in leaves from LS (a) and YS (b) during rice filling and maturity.
Plants 13 02018 g004
Table 1. Basic physical and chemical properties of soils.
Table 1. Basic physical and chemical properties of soils.
Soil TypeCdpHTotal Ca Ca2+Total Mg Mg2+CO32−
(mg·kg−1) (g·kg−1)(g·kg−1)(g·kg−1)(g·kg−1)(mg·kg−1)
YS0.675.853.250.551.720.4310.76
LS0.697.085.462.052.810.90 42.29
Table 2. DTPA Cd content of LS and YS in different treatments during rice filling and maturity (mg·kg−1).
Table 2. DTPA Cd content of LS and YS in different treatments during rice filling and maturity (mg·kg−1).
Soil TypeCd LevelFilling IFilling IIFilling IIIMaturity
LSLS10.144 ± 0.032 g0.271 ± 0.017 f0.288 ± 0.015 f0.177 ± 0.025 f
LS20.547 ± 0.089 e0.585 ± 0.018 d0.654 ± 0.056 d0.542 ± 0.058 d
LS30.998 ± 0.013 c1.000 ± 0.030 c1.013 ± 0.072 c0.913 ± 0.082 c
LS41.754 ± 0.077 a 1.986 ± 0.092 a2.053 ± 0.076 a1.864 ± 0.119 a
YSYS10.094 ± 0.012 g0.108 ± 0.021 g0.122 ± 0.018 g0.077 ± 0.022 f
YS20.405 ± 0.037 f0.426 ± 0.031 e0.473 ± 0.014 e0.350 ± 0.050 e
YS30.754 ± 0.020 d0.635 ± 0.025 d0.686 ± 0.036 d0.602 ± 0.052 d
YS41.462 ± 0.043 b1.372 ± 0.073 b1.432 ± 0.089 b1.351 ± 0.064 b
The results of this study are expressed as mean (mg·kg−1) ± standard error (n = 3), superscripts (a–g) indicate significant differences between different categories of samples (LSD test, p < 0.05), and the same letters indicate no significant differences between samples.
Table 3. Total Ca and Mg content of LS and YS in different treatments during rice filling and maturity (g·kg−1).
Table 3. Total Ca and Mg content of LS and YS in different treatments during rice filling and maturity (g·kg−1).
Soil TypeCd LevelFilling IFilling IIFilling IIIMaturity
CaMgCaMgCaMgCaMg
LSLS15.16 ± 0.12 a2.46 ± 0.13 a5.15 ± 0.21 a2.54 ± 0.20 a5.26 ± 0.07 a2.54 ± 0.29 a5.05 ± 0.18 a2.45 ± 0.15 a
LS24.90 ± 0.25 a2.24 ± 0.18 a5.03 ± 0.33 a2.46 ± 0.38 a5.02 ± 0.23 a2.33 ± 0.14 a5.13 ± 0.12 a2.33 ± 0.47 ab
LS34.73 ± 0.16 a2.13 ± 0.08 a4.92 ± 0.11 a2.24 ± 0.03 a4.93 ± 0.22 a2.20 ± 0.03 a4.58 ± 0.07 a2.13 ± 0.07 a
LS44.63 ± 0.01 a1.96 ± 0.04 a4.62 ± 0.23 a1.96 ± 0.07 a4.63 ± 0.16 a1.90 ± 0.04 a4.24 ± 0.16 a1.85 ± 0.02 a
YSYS12.86 ± 0.21 b1.53 ± 0.08 b2.84 ± 0.21 b1.57 ± 0.21 b3.03 ± 0.22 b1.74 ± 0.14 b2.92 ± 0.09 b1.73 ± 0.02 b
YS22.60 ± 0.13 bc1.45 ± 0.10 bc2.69 ± 0.04 bc1.45 ± 0.18 bc2.30 ± 0.18 bc1.48 ± 0.08 bc2.35 ± 0.09 bc1.46 ± 0.37 bc
YS32.50 ± 0.03 c1.25 ± 0.11 bc2.51 ± 0.02 c1.24 ± 0.06 bc2.22 ± 0.52 bc1.20 ± 0.03 bc2.70 ± 0.24 bc1.23 ± 0.03 bc
YS42.04 ± 0.08 c1.05 ± 0.04 c2.06 ± 0.16 c1.09 ± 0.04 c1.99 ± 0.14 c1.00 ± 0.05 c2.09 ± 0.10 c0.90 ± 0.20 c
The results of this study are expressed as mean (mg·kg−1) ± standard error (n = 3), superscripts (a–c) indicate significant differences between different categories of samples (LSD test, p < 0.05), and the same letters indicate no significant differences between samples.
Table 4. Total Ca and Mg content of rice plants in different treatments at maturity (mg·kg−1).
Table 4. Total Ca and Mg content of rice plants in different treatments at maturity (mg·kg−1).
Soil TypeCd LevelRootStemLeaveGrain
CaMgCaMgCaMgCaMg
LSLS11226 ± 1412323 ± 752079 ± 1602942 ± 1261980 ± 211769 ± 67294 ± 52954 ± 153
LS21402 ± 962446 ± 922253 ± 623083 ± 2902042 ± 212087 ± 48321 ± 611051 ± 44
LS31520 ± 782876 ± 1812386 ± 883462 ± 2082159 ± 712057 ± 45287 ± 541205 ± 154
LS41895 ± 2253075 ± 572800 ± 1053613 ± 352201 ± 1722347 ± 194276 ± 481155 ± 96
YSYS1948 ± 1181953 ± 1532056 ± 722480 ± 1521747 ± 371351 ± 113394 ± 80779 ± 140
YS21134 ± 1742238 ± 1222290 ± 542701 ± 451799 ± 1231644 ± 80336 ± 501015 ± 101
YS31379 ± 1052401 ± 1022788 ± 723058 ± 1251898 ± 971961 ± 5327 ± 691038 ± 37
YS41659 ± 1252625 ± 553021 ± 2353427 ± 1792051 ± 722163 ± 128251 ± 51091 ± 48
The results of this study are expressed as mean (mg·kg−1) ± standard error (n = 3).
Table 5. Correlation between CRIs and DTPA Cd in soil.
Table 5. Correlation between CRIs and DTPA Cd in soil.
DTPA CdCa2+Mg2+Total AlkalinitypH
DTPA Cd1−0.347 *−0.335 *−0.320 *−0.346 *
Ca2+−0.14710.2120.746 **0.817 **
Mg2+−0.1950.21210.566 **0.498 **
Total alkalinity−0.2200.746 **0.566 **10.966 **
pH−0.2460.817 **0.498 **0.966 **1
** The correlation was significantly different at 0.01 level (two-tailed); * the correlation was different at 0.05 level (two-tailed).
Table 6. Correlation between Ca2+ and Mg2+ content in soil and Cd content in different parts of rice.
Table 6. Correlation between Ca2+ and Mg2+ content in soil and Cd content in different parts of rice.
Pearson Correlation CoefficientRootStemLeafGrain
Ca2+Filling stage I−0.211−0.332−0.377−0.240
Filling stage II0.010−0.243−0.3200.000
Filling stage III−0.122−0.301−0.320−0.356
Maturity−0.353−0.596−0.516−0.779 *
Mg2+Filling stage I−0.438−0.623−0.631−0.444
Filling stage II−0.307−0.561−0.620−0.335
Filling stage III−0.599−0.722 *−0.777 *−0.769 *
Maturity−0.095−0.341−0.271−0.495
* The correlation was different at 0.05 level (two-tailed).
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Wang, H.; Teng, L.; Mao, X.; He, T.; Fu, T. Comparing the Effects of Lime Soil and Yellow Soil on Cadmium Accumulation in Rice during Grain-Filling and Maturation Periods. Plants 2024, 13, 2018. https://doi.org/10.3390/plants13152018

AMA Style

Wang H, Teng L, Mao X, He T, Fu T. Comparing the Effects of Lime Soil and Yellow Soil on Cadmium Accumulation in Rice during Grain-Filling and Maturation Periods. Plants. 2024; 13(15):2018. https://doi.org/10.3390/plants13152018

Chicago/Turabian Style

Wang, Hu, Lang Teng, Xu Mao, Tengbing He, and Tianling Fu. 2024. "Comparing the Effects of Lime Soil and Yellow Soil on Cadmium Accumulation in Rice during Grain-Filling and Maturation Periods" Plants 13, no. 15: 2018. https://doi.org/10.3390/plants13152018

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