Abstract
Pot experiments were conducted to study the effects of rice straw (RS), rice straw ash (RSA), and bone charcoal (BC) on the bioavailability of 15 rare earth elements (REEs) in soil and the absorption and accumulation of REES by rice. Adding RSA and BC to REE-contaminated soil remarkably increased the biomass and yield of rice, and the addition of RS remarkably inhibited the growth of rice. Compared with the control check (CK), the total REE concentration in the soil solution at the tillering stage, heading stage, and maturity stage was significantly increased by adding RS, and the total REE concentration in the soil solution was remarkably decreased by adding RSA and BC. The concentration of 15 REEs in the roots, shoots of rice, and brown rice were remarkably decreased via RSA addition. The concentration of total REEs in rice roots, shoots, and grains decreased 79.1%, 76%, and 18.3%, respectively, and the concentration of total REEs in the roots and shoots of rice decreased 19.9% and 67.2%, respectively via RSA addition. However, there was no noticeable effect on the concentration of total REEs in brown rice. So BC and RSA are suitable to be added to REE-contaminated soil, but RS is not.
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Effects of Rice Straw, Rice Straw Ash, and Bone Charcoal on Uptake and Accumulation of Rare Earth Elements in Rice Plants
Shulan Jin,a Zhongjun Hu,a Yizong Huang,b,* Huahua Pan,a and Ying Hu c
Pot experiments were conducted to study the effects of rice straw (RS), rice straw ash (RSA), and bone charcoal (BC) on the bioavailability of 15 rare earth elements (REEs) in soil and the absorption and accumulation of REES by rice. Adding RSA and BC to REE-contaminated soil remarkably increased the biomass and yield of rice, and the addition of RS remarkably inhibited the growth of rice. Compared with the control check (CK), the total REE concentration in the soil solution at the tillering stage, heading stage, and maturity stage was significantly increased by adding RS, and the total REE concentration in the soil solution was remarkably decreased by adding RSA and BC. The concentration of 15 REEs in the roots, shoots of rice, and brown rice were remarkably decreased via RSA addition. The concentration of total REEs in rice roots, shoots, and grains decreased 79.1%, 76%, and 18.3%, respectively, and the concentration of total REEs in the roots and shoots of rice decreased 19.9% and 67.2%, respectively via RSA addition. However, there was no noticeable effect on the concentration of total REEs in brown rice. So BC and RSA are suitable to be added to REE-contaminated soil, but RS is not.
Keywords: Rice straw; Rice straw ash; Bone charcoal; Rare earth elements; Rice plants
Contact information: a: Shangrao Normal University, Shangrao, China, 334000; b: Agro-Environment Protection Institute of the Ministry of Agriculture, Tianjing, China; 300191; c: Research Center for Eco-Environmental Sciences, Chinese Academy of Science, Beijing, China, 100085;
* Corresponding author: yizonghuang@126.com
INTRODUCTION
Rare earth element (REE) is the general term used for the members of the third subgroup B elements (IIIB) family in the periodic table, i.e., scandium, yttrium, and the lanthanides. The lanthides are the 15 chemical elements with atomic numbers 57 through 71 (Cornell et al. 1993; Zhao and Wilkinson 2015). The properties of REEs are very similar in three ways: (1) the atomic structure is similar; (2) the ionic radius is similar; and (3) the common valence is +3, which allows stable coordination compounds to form easily. Thus, they are closely symbiotic in nature (Hu et al. 2006; Aquino et al. 2009). The most common grouping method for REEs is dichotomy, namely by light REEs and heavy REEs. Light REEs are also known as cerium REEs and include La through Eu on the periodic table. Heavy REEs, also known as yttrium rare earth, include Gd through Lu, Y, and Sc (Wyttenbach et al. 1998; Tyler 2004; Wiche et al. 2016). China, mainly South China with South Jiangxi as its center, is rich in rare earth resources (especially ionic-type rare earth resources), accounting for 90% of the global supply of rare earth resources. During the process of the exploitation and smelting of rare earth resources, the REE enrichment of soil, water, and the crops surrounding the mining areas becomes higher due to the lack of supervision, illegal exploitation, outdated technology, and emission of the industrial “Three Wastes” (waste gas; waste water; industrial residue) (Pan and Zhu 2003; Jin and Huang 2013, 2014; Wiche et al. 2016; Suja et al. 2017; Zhuang et al. 2017). Rare earths are not necessary nutrients for the growth of plants and animals. Small amounts of REEs can promote growth, yet large amounts can inhibit growth and even lead to poisoning (Jin et al. 2016; Wiche et al. 2016; Gravina et al. 2018; Zheng et al. 2018). With the extensive use of REEs in many industries, the accumulation of rare earths in the environment is steadily getting worse, and REEs enter the human body through the consumption of food (Wang et al. 2017; Kyra et al. 2017). It has been reported that the concentrations of REEs in the hair, blood, bone, brain, and liver of residents of mining areas are remarkably higher than those in non-mining areas (Wei et al. 2013; Li et al. 2014). This affects the health of the mining area residents, as shown via abnormal biochemical indices of the blood, abnormal functioning of the liver, and lower IQ of children living in mining areas. High concentrations of REEs also adversely affect functions of the reproductive and immune systems (Zhang et al. 2000; Li et al. 2014; Liu et al. 2015). However, few studies have been done on how to reduce the uptake of REEs into the food chain from the soil.
South China (with South Jiangxi as its center) is an important global area for ionic rare earth distribution. The main soil in South Jiangxi is red soil, which is acidic and lacks organic manure and effective phosphate. The area is also an important grain-producing area, as hundreds of millions of tons of rice straw are produced annually. Rice straw is composed of large amounts of organic matter and inorganic matter. The organic matter is composed of cellulose and soluble organic matter. The silicate concentration of inorganic substances is higher than 12% (Ma et al. 2002). To avoid environmental pollution and the waste of resources, rural rice straw is generally returned to the field and used comprehensively. The return of rice straw to the field can increase the soil organic manure and improve soil properties and soil nutrients. There are two main forms of comprehensive utilization of rice straw: electricity generation viagasification and rice straw burning. The burning of rice straw forms a large amount of rice straw ash. The RSA is alkaline, contains potassium oxide, and, of particular note, comprises more than 70% silica (Ma et al. 2002). The addition of RSA to red soil can improve the soil properties and nutrient contents.
To date, many studies have examined the effects of dissolved organic matter (DOM), phosphorated material, and silicate on the form and availability of heavy metals in the soil for China and the rest of the world. Returning rice straw to fields can increase soil organic matter and form DOM. Dissolved organic matter is a negatively charged colloid that competes with heavy metals in soil. It can promote the dissolution and desorption of heavy metals in the soil and become a “carrier” in heavy metal migration and activation, thus affecting the bio-availability of heavy metals in the environment (Zhu et al. 2014, 2016; Rikta et al. 2018). Xu and Yuan found that as the DOM concentration increased, the concentration of water-soluble heavy metals in the soil gradually increased (Xu and Yuan 2009). Jin et al. (2016) found that the formation of DOM in soil resulted in a significant increase in the concentration of water-soluble REEs. In contrast, DOM has the ability to form complexes with heavy metals because it has a large number of functional groups, such as carboxyl, hydroxyl, and carbonyl groups. Organic matter can also form complexes with heavy metals by using Fe or S as a bridge directly or indirectly, thus reducing the mobility of heavy metals in soil (Perroeenet et al. 2000; Williams et al.2011). The DOM can affect the bio-availability of heavy metals from two distinct aspects. Many studies have shown that siliceous ions react with heavy metals to form silicic acid precipitates when silicon-containing materials are applied to soil. Silicon-containing materials can increase the pH of soil, enhance the soil adsorption capacity, adsorb heavy metal ions or complexes with opposite charges in soil, and reduce the activity of heavy metals (Zhao et al. 2014; Rizwan et al. 2016a; Gao et al. 2018; Talitha et al. 2018). Silicon is an important component of cell walls. The silicon present in cell walls binds to Cd, attaching it to cell walls. Adding silicon to soil can enhance the cell wall retention of Cd in soil organisms (Liu et al. 2013; Duan et al. 2016). After bone charcoal is added to soil, the phosphoric acid ions in plant roots generated via the acidic soil can form a refractory metal phosphate with the REE ions. Bone charcoal is alkaline and has alkali ions, a large surface area, and abundant functional groups that contribute to metal complexation (Rinklebe et al. 2016; Rizwan et al. 2016b). The effects of bone charcoal when added to soil include the immobilization of heavy metals, modification of soil pH, and improvement in the physical and biological properties of soil (Rizwan et al. 2016b). However, it is not known whether the effects of soil organic matter, silicon-containing materials, and phosphorus-containing materials on the bio-availability of heavy metals fully reflect the impacts on the bio-availability of REEs. Hence, it is necessary to scientifically evaluate the effects of organic matter, silicon-containing materials, and phosphorus-containing materials on the yield, quality, and ecological environment of rice fields in rare earth mining areas. Furthermore, it is necessary to explore the rational restoration methods of rare-earth-contaminated soil, and provide guidance for the theory and practice of food safety, ecological environment protection, and the rational utilization of straw in rare earth mining areas.
EXPERIMENTAL
Materials
The test soil was collected from the rare-earth mine in the town of Jiading, Xinfeng County, Ganzhou City, Jiangxi Province, China. The soil sampling occurred as follows: the top 20 cm of soil was collected, dried naturally, removed of stones and plant residue, crushed, passed through a 100-mesh sieve, and stored until use. The physical and chemical properties of the soil and REE concentrations are shown in Table 1. The test rice straw (RS) was collected from the Xinzhou District of Jiangxi Province, China, which does not suffer rare earth pollution, and crushed into powder by a powder machine (Shanghai Precision Science Instrument Co., Ltd., Shanghai, China). The rice straw ash (RSA) was purchased from the Longshui Plant Straw Processing Plant in Ganyu County (Lianyungang, China). The bone charcoal (BC) was bought from the Tengzhou Chemical Plant in Shandong Province (Zaozhuang, China). The physical and chemical properties of the RS, RSA, and BC and their concentrations of REEs are shown in Table 1.
The rice variety was Jin Qian 47, and the rice seed was purchased from Jinhua Agricultural Science Institute of Zhejiang Province (Jinhua, China). The seeds were sterilized in a 10% H2O2 solution for 10 min, then washed with water several times. The seeds were planted in the test soil (free from rare earth pollution) for seedling raising.
Treatments
Pot experiments were conducted to study the effects of different soil amendments on the absorption and accumulation of REEs in rice. Four treatments were set: control group without modifier addition (CK), 2.5% rice straw (RS), 2.5% rice straw ash (RSA), and 2.5% bone charcoal (BC), with each treatment performed in triplicate.
Table 1. Physicochemical Properties and REEs Concentrations of Soil and Amendments
Notes: RS refers to rice straw, RSA refers to rice straw ash (RSA), and BC refers to bone charcoal.
In the experiment, a plastic basin with a height of 26 cm and a diameter of 24 cm was used, to which 5 kg of soil was added. To grow the rice plants, 5.4 g of urea (containing 46.6% N) and 0.6 g of potassium chloride (containing 62.9% K2O) were used as fertilizer. According to the experimental design, the additives are added into the tested soil and stirred thoroughly until the additives are evenly distributed in the soil. An even mixture of soil amendments and the test soil was added into each plastic basin. The water balance was maintained for two weeks, and the water level was maintained at approximately 3 cm.
After three weeks of growth, the rice seedlings were transplanted to culture pots, with two seedlings per pot. After the transplantation, a soil solution extractor was embedded in each culture pot, deep in the rhizosphere of the rice, and used to collect the soil solution samples. The pot experiment was conducted in a greenhouse. The growth conditions of rice were cycles of light at 28 ℃ for 14 h and darkness at 20 ℃ for 10 h, luminous intensity of 260 to 350 mol·m-2·s-1, and relative humidity of 60% to 70%. To ensure the uniformity of light and heat received per pot of rice, the position of each pot of rice was randomly changed every three days. During the entire test period, the soil in the basin remained flooded. The soil solution was collected at the tillering, heading, and maturity stages of rice and then filtered with a 0.45-m filter membrane.
After 1% nitric acid acidification, the solution was preserved in a refrigerator at 4 ℃ prior to testing. After the rice ripened, it was harvested. First, the rice was dropped manually from the rice panicle and loaded into a net bag. Then, the shoots and roots of the rice were harvested separately and rinsed with tap water first followed by three rinses with deionized water.
Water-absorbent paper was used to remove any leftover water by drying it to a constant weight in a 70 ℃ oven. The harvested rice was placed in an indoor area with ventilation and dried naturally; then, the husk was removed by a sheller and the grains collected. A stainless-steel grinder was used to grind the grains, shoots, and roots into powder, which was then stored at room temperature until analysis.
Table 2. Effects of Different Amendments on the Concentrations of Rare Earth Elements in Different Parts of Rice
Note: The concentration unit of rare-earth elements in rice roots and shoots was mg.kg-1, and the concentration unit in the grain of rice was μg.kg-1. Data represent the average (n = 3); different lowercase letters on same line in the different parts of the rice indicate that the difference between treatment was significant (p < 0.05); RS refers to rice straw, RSA refers to rice straw ash (RSA), and BC refers to bone charcoal, CK refers to control check.
Table 3. Effects of Amendments on the Concentration of REEs (μg.L-1) in Soil Solutions at Different Growth Stages in Rice
Note: Data is the average (n = 3), different lowercase letters in the same growing period of rice indicate that the difference between treatment is significant (p < 0.05); RS refers to rice straw, RSA refers to rice straw ash (RSA), and BC refers to bone charcoal, CK refers to control check.
Methods
Analysis of physical and chemical properties of soil samples
The soil pH was determined via the electrode method with a soil to water ratio of 2.5:1. The soil organic matter content was determined using the low-temperature external heat-potassium dichromate colorimetric method. The soil cation exchange concentration (CEC) was determined via the ammonium acetate method. The total concentrations of soil carbon, nitrogen, and sulfur were determined using an elemental analyzer (Vario EL III, Elementar, Frankfurt, Germany); and the texture composition was determined using a laser particle size analyzer (Zhuhai Omec Instrument Co., Ltd., Zhuhai, China).
Digestion of soil samples and determination of the total amount of REEs
In a quartz glass tube, 0.2 g soil samples were mixed with 5 mL aqua regia (HNO3:HCl = 3:1). The mixture was incubated at room temperature overnight and then digested in an open digestion furnace the next day. The digestion temperature control program consisted of digestion at 90 ℃ or 30 min at 120 ℃ for 4 h, and at 140 ℃ until the soil turned white. After the digestion, the samples were placed in a ventilator to volatilize the acid and then transferred to 50-mL fixed-volume tubes. The samples were filled with ultrapure water to 50 mL, shaken well, filtered with a 0.45-µm filter membrane, and analyzed via inductively coupled plasma mass spectrometer (ICP-MS) (Agilent Technologies Inc., Palo Alto, CA, USA). The whole process of digestion was calibrated based on a national standard substance (GBW07405, National Standard Substance Research Center, Beijing, China).
Plant sample digestion and determination
A total of 0.2 g of the crushed plant sample was placed in a 50-mL polytetrafluoroethylene digestion tank, and then 3 mL high-grade pure nitric acid was added and mixed in evenly. The mixture was incubated at room temperature overnight, and then digested in a microwave digestion furnace (MARS5, CEM Microwave Technology Ltd., Matthews, NC, USA) the next day. First, the samples were heated to 120 ℃, which was maintained for 5 min, and then the temperature was increased to 160 ℃, which was maintained for 15 min. The whole process of digestion was controlled by a national standard substance (GBW08502, National Standard Substance Research Center, Beijing, China). After digestion, the samples were placed in a ventilated kitchen to cool and for acid removal, and then fixed to 40 mL, filtered through a 0.45-µm filter membrane, and finally analyzed via ICP-MS. The concentrations of P in the soil, rice roots, stems, and grain digestion solutions were determined via molybdenum-antimony resistance and ultraviolet-visible spectrophotometry (Shanghai Precision Science Instrument Co., Ltd., Shanghai, China).
Data analysis
The ability of rice roots to transfer rare earths to shoots is expressed by the translocation factor (TF) as follows: TF (%) = CShoot-REE/CRoot-REE × 100.
The data were analyzed using Origin 9.0 (Origin Lab, Hampton, USA), SPSS 19.0 (SPSS Inc., Chicago, IL, USA), and Excel 2007 (Microsoft, Redmond, WA, USA) software, and the single factor variance (ANOVA) and Duncan test methods were used for significance analysis (p < 0.05). A bivariate correlation was used for the Pearson analysis.
RESULTS AND DISCUSSION
Effect of Different Modifiers on the Growth of Rice
According to Figs. 1 and 2, rice with the RSA and BC addition grew the best, and rice with the RS addition grew the worst. Rice straw, ash, and bone charcoal promoted rice growth in rare-earth-contaminated soil. The dry weights of the rice roots, shoots, and grains with RSA addition increased 124.5%, 91.3%, and 103.1%, respectively, compared with those of the CK treatment; and those with BC addition increased 101.8%, 82.6%, and 100.5%, respectively, compared with those of CK. The rice straw inhibited the growth of rice in the rare-earth-contaminated soil. The dry weights of the rice roots, shoots, and grains decreased 62%, 69.3%, and 82.5%, respectively, compared with those of CK.
Fig. 1. The effect of different modifiers on the growth of rice (heading stage)
Effects of Different Modifiers on the Concentrations of Rare Earth Elements and P in Rice
Table 2 illustrates that the RS, RSA, and BC significantly affected the REE concentration in the roots of rice. The concentrations of REEs in the rice roots with the RS addition were significantly higher than those of the control; for instance, the concentrations of Ho, Pr, and Y were 221.5%, 86.5%, and 42.1% higher than those of CK, respectively. The average value of light REEs (La through Eu) increased 17.1%, and that of heavy REEs increased 24.9%. The total rare earth concentration of rice roots was reduced 19.9% compared to CK, whereas the concentrations of Pr, Dy, Sm, Y, La, Ce, Nd, Eu, and Gd as single REEs were significantly lower than those of the control (P < 0.05). In particular, the concentrations of Pr, Dy, and Sm were reduced 68.8%, 64.7%, and 39.9%, respectively. The effect of adding BC was the most significant.