Medicago sativa L. enhances the phytoextraction of cadmium and zinc by Ricinus communis L. on contaminated land in situ

Ecological Engineering Volume 116, June 2018, Pages 61-66 Ecological Engineering Author links open overlay panelPeng-pengXiongabChi-quanHeabOHKokyocXuepingChenbXiaLiangbXiaoyanLiubXueChengbChang-luWuabZheng-chiShiab https://doi.org/10.1016/j.ecoleng.2018.02.004 Get rights and content Abstract Crop co-planting is widely used in agriculture because it can increase total crop yields through increased resource use efficiency, and phytoremediation is based on the contaminant remediation system in plants. This study focused on the phytoextractive effects of co-planting Ricinus communis and/or legumes in Cd- and Zn-contaminated soil. A Cd- and Zn-contaminated factory relocation site in Shanghai was selected for the experiment, and according to the results of a potential ecological risk assessment of heavy metals, the study area was divided into 3 levels of pollution: slight, moderate, and high. The results showed that the presence of Medicago sativa can significantly increase the height and biomass of R. communis, and there was a greater impact on the chlorophyll content of R. communis at higher pollution levels. Differences in pollution levels could significantly change the oil content of R. communis plants, but M. sativa can alleviate the impact of heavy metals. The presence of M. sativa increased the cumulative amount of cadmium and zinc in R. communis by 1.14 and 2.19 times, respectively. In short, co-planting R. communis and legumes remediated contaminated soil and may be one practical phytoremediation pathway for heavy metal-contaminated soil in the future. Previous article Next article Keywords Plant coexistence Phytoextraction Cadmium Zinc Ricinus communis L. Medicago sativa L. 1. Introduction As the world has undergone industrial economic growth, heavy metals have gradually accumulated in agricultural soils. It is said that more than 16.1% of soils in China are contaminated, including 7.0% with cadmium (Cd) and 0.9% with zinc (Zn) (Chen et al., 2016). Therefore, the remediation of contaminated soil is necessary to save land resources and protect human health (Kramer, 2005; Vangronsveld et al., 2009). Phytoremediation is based on the contaminant remediation system in plants, and it has recently become an economically, environmentally and aesthetically accepted technology (Ahmadpour et al., 2012; Conventionally, 2011; Majid et al., 2012). Ricinus communis L. is an oilseed crop in the Euphorbiaceae family (Wale and Assegie, 2015) that has a high biomass and a well-developed root system. China produces the second largest amount of R. communis in the world (Bauddh and Singh, 2015), and the crop is also metal tolerant, with a high tolerance to Cd concentrations (Shi and Cai, 2009). R. communis has a higher remediation efficiency than Indian mustard (Brassica juncea L.), which is considered a potential phytoremediator (Bauddh and Singh, 2012), and it has a high phytoremediation potential for cadmium- and zinc-contaminated soils (Wang et al., 2016). However, fast-growing and high biomass plants often contain low to moderate concentrations of heavy metals (McGrath et al., 2001). Thus, researchers have studied several approaches to improve the potential for heavy metal phytoextraction using R. communis. One idea was to apply metal chelators, but some chemical chelators are relatively expensive and present environmental risks (Wu et al., 2006). In addition, a low concentration of chemical chelators can reduce plant biomass (Chen and Cutright, 2001). Furthermore, plants can increase metal bioavailability by themselves; experiments have shown that some plant roots can produce H+ and small-molecular-weight organic acids that can increase the amount of bioavailable metals (Duarte et al., 2007). Crop co-planting has been widely used in agriculture in China for 2000 years (Zhang and Li, 2003), and legumes are often included in such systems because of their ability to fix N2 (Karpenstein-Machan and Stuelpnagel, 2000; van Kessel and Hartley, 2000). In this study, we assumed that N-fixers can provide additional N to the main crop plant, which can produce substantial biomass and thus enhance the phytoextraction of cadmium and zinc from contaminated soil. We used Medicago sativa L. as the legume species to intercrop with R. communis because it is a metal-tolerant plant that can tolerate both zinc and cadmium (Desjardins et al., 2016; Kabir et al., 2016). We focused on the phytoextraction of cadmium and zinc from contaminated soil, and our main objectives were to investigate (i) whether co-planting with the legume affected the chlorophyll and oil contents of R. communis, (ii) whether co-planting with the legume affected the growth and biomass of the phytoextractor (R. communis), and (iii) whether co-planting with the legume enhanced the phytoextraction of cadmium and zinc by R. communis. 2. Materials and methods 2.1. Field experiment The field experiment was implemented in a 200-m2 area of a factory relocation site in Shanghai (31°11′42″ N; 121°32′35″ E); the properties of the soil are described in Table 1. The field experiment was divided into thirty-six plots with an area of 1.5 m × 3 m each. Surface soil (0–20 cm) was collected to determine the Zn and Cd concentrations in each plot; the heavy metal concentration range is presented in Table 1. Based on the heavy metal concentration in each block, the Hakanson potential ecological risk assessment was used. RI was introduced to assess the degree of ecological risk of heavy metals in the soil and was calculated using the following equation: where RI is the sum of the potential risk of individual heavy metals; Ei r is the potential risk of individual heavy metals; Ti f is the toxic-response factor for a given heavy metal; Ci f is the contamination coefficient; Ci s is the current concentration of heavy metals in the soil; and Ci n is the pre-industrial record of the heavy metal concentration in the soil. Table 1. Soil properties. pH 7.62 Organic matter (mg kg−1) 18777 Total N (mg kg−1) 836 Total P (mg kg−1) 548 Total Cd (mg kg−1) 0.32–2.77 Total Zn (mg kg−1) 152–1427 According to the results of the potential ecological risk assessment of heavy metals, the area was divided into three different pollution levels (Hakanson, 1980): slight (RI 〈1 5 0), moderate (150 ≤ RI 〈3 0 0), and high (300 ≤ RI). The experiment employed a two-factorial design with three different pollution levels and two plant types, R. communis alone and R. communis co-planted with M. sativa. The planting layout is shown in Fig. 1, and the corresponding plants were seeded in each plot according to the schematic. The seeding date was May 24, and the number of plant seeds sown were 5 grains of R. communis and 20 grains of M. sativa. All the seeds were sourced from the Shanghai market. Download high-res image (89KB)Download full-size image Fig. 1. The arrangement of R. communis and M. sativa experimental plats. Rs: Ricinus communis L. + Slight level of pollution, Rm: Ricinus communis L. + Moderate level of pollution, Rh: Ricinus communis L. + High level of pollution, RMs: Ricinus communis L. + Medicago sativa L. + Slight level of pollution, RMm: Ricinus communis L. + Medicago sativa L. + Moderate level of pollution, and RMh: Ricinus communis L. + Medicago sativa L. + High level of pollution. 2.2. Plant harvest analysis Plants were harvested 120 days after sowing, and the height and stem circumference at 15 cm of R. communis were measured with a metric scale. Plants were divided into roots, stems, leaves and fruits, which were washed with deionized water for further analysis. 2.3. Chlorophyll concentrations Fresh leaf tissues (approximately 0.2 g) were cut in color-comparison tubes. Then, the samples were kept in 25 ml of 80% acetone and 95% ethanol (v:v = 2:1) for 24 h for complete extraction, and the total chlorophyll concentrations of R. communis were determined spectrophotometrically using the visible wavelength of 652 nm. 2.4. Oil content of fruits The oil contents of fruits were determined by the Soxhlet extraction method. Fruits were dried in an oven at 70 °C for 48 h and then ground and passed through 0.25-mm sieves. Three-gram porphyrization samples were loaded into a weighed filter bag; the mouth of the package was sealed; and the samples were dried in a 105 + 2 °C oven for 3 h. The extraction barrel was placed with the sample, and petroleum ether was added. Samples were extracted for 12 h and kept at a water temperature of 70 °C. After extraction, the petroleum ether was volatilized in a ventilated area, and the samples were then dried in the 105 + 2 °C oven for 2 h and weighed. 2.5. Elemental analysis Roots, stems, leaves and fruits were oven-dried at 105 °C for 30 min and then at 70 °C for 48 h. Dry biomass was powdered and digested (Liu et al., 2008), and the Cd and Zn concentrations were determined using ICP-AES (ICP, LEEMAN Company, United States) and AAS (ZEEnit600, Analytik Jena AG, Germany). Soils were air-dried and passed through 0.25-mm sieves. The Cd and Zn concentrations from the soil samples were digested and analyzed by ICP-AES (ICP, LEEMAN Company, United States) and AAS (ZEEnit600, Analytik Jena AG, Germany). 2.6. Bioconcentration factor (BCF) The bioconcentration factor (BCF) was used to evaluate the efficiency of Cd and Zn phytoextraction, and it was calculated using the following equation: where Cplant (mg/kg) is the heavy metal concentration of the plant, including the roots, stems and leaves, and Csoil (mg/kg) is the heavy metal concentration in the soil (Ghosh and Singh, 2005). 2.7. Statistical analysis Data were analyzed by two-way ANOVA with Duncan’s test (p < 0.05) using SPSS 17.0 for Windows (SPSS Inc. IBM Corporation, Armonk, NY, USA). 3. Results 3.1. Influence of co-planting on R. communis growth Co-planting with M. sativa significantly increased the height of R. communis, and the influence was greatest under slight pollution levels. It could be that M. sativa performed nitrogen fixation during growth, providing N to and promoting the growth of R. communis. The height of R. communis was not significantly impacted by different levels of pollution, indicating that this species exhibited strong tolerance to heavy metal toxicity (Fig. 2A, Table 2). Download high-res image (300KB)Download full-size image Fig. 2. The effects of different treatments on the average height (A), stem circumference (B) and biomass (C) of Ricinus communis L. (n ≥ 3). Different letters indicate significant differences according to LSD at p < 0.05. Table 2. F values of the variation in R. communis L. plant height, circumference, biomass, chlorophyll, and oil content in relation to the presence of M. sativa and pollution level. Variables Plant height Circumference Biomass Chlorophyll Oil content M. sativa 6.20* 4.38* 2.42* 0.86* 0* Pollution level 0.85 0.68 0.44 2.98* 0.46* M. sativa × Pollution level 0.61 0.3 0.13 0.35 0.45 * p < 0.05 The circumference of R. communis stems was measured at a height of 15 cm, and it was greater with M. sativa than without, indicating that the presence of M. sativa can significantly influence the growth of R. communis. The stem circumference of R. communis with M. sativa was largest under slight levels of pollution (Fig. 2B, Table 2). Fig. 2C shows that the different treatments affected the biomass of R. communis L., but different pollution levels did not. The presence of M. sativa can significantly increase the biomass of R. communis (Table 2), which was highest under slight levels of pollution. The biomass of R. communis with M. sativa reached 881 g and increased by nearly 80%. Therefore, M. sativa significantly affected the height, circumference and biomass of R. communis. However, the effect of different pollution levels on these same variables was not significant. 3.2. Chlorophyll concentrations Where heavy metal pollution was more severe, the influence of R. communis on chlorophyll was greater. High levels of pollution decreased the chlorophyll content of R. communis L., but co-planting with M. sativa alleviated the impacts on chlorophyll under moderate levels of pollution. High levels of pollution can significantly affect the chlorophyll content of R. communis planted with M. sativa, and the chlorophyll content of R. communis was highest when planted with M. sativa (2.47 mg/g) (Fig. 3, Table 2). Download high-res image (139KB)Download full-size image Fig. 3. The effects of different treatments on the chlorophyll content of Ricinus communis L. (n ≥ 3). Different letters indicate significant differences according to LSD at p < 0.05. 3.3. Oil content of fruit The oil content of the fruit of R. communis planted with M. sativa was not affected by different levels of pollution. Generally, pollution can significantly change the oil content of R. communis fruit; high levels decreased the oil content of R. communis fruit by 9.8%. The highest oil content of R. communis fruit without M. sativa was 43% under slight levels of pollution (Fig. 4, Table 2). Download high-res image (155KB)Download full-size image Fig. 4. The effects of different treatments on the oil content of Ricinus communis L. (n ≥ 3). Different letters indicate significant differences according to LSD at p < 0.05. 3.4. Elemental analysis Fig. 5A shows that R. communis accumulated cadmium, of which the average accumulation was 0.9867 mg in R. communis without M. sativa and 1.1257 mg with M. sativa; the latter is 1.14 times the former. Different treatments did not affect the accumulation of cadmium in the ground portion of R. communis, which had far greater cadmium accumulation than the belowground portion. Different pollution levels did not significantly impact the cadmium accumulation of R. communis roots without M. sativa, but when M. sativa was present, it alleviated the heavy metal poisoning of R. communis roots. Download high-res image (303KB)Download full-size image Fig. 5. The effects of different treatments on heavy metal accumulation by Ricinus communis L. (n ≥ 3). Shoots accumulated heavy metals above the abscissa, and roots accumulated heavy metals below the abscissa. Different letters indicate significant differences according to LSD at p < 0.05. According to the chart in Fig. 5B, R. communis accumulated zinc with an average accumulation of 32.4707 mg in R. communis without M. sativa and 71.1968 mg with M. sativa; the latter is 2.19 times the former. The amount of zinc accumulated by R. communis in the ground portion was far greater than that by the belowground portion. M. sativa promotes zinc accumulation in R. communis shoots, of which the quantity was significantly affected by different pollution levels. The different treatments did not affect zinc accumulation by R. communis roots. 3.5. Bioconcentration factor (BCF) Different treatments did not affect the Cd content of R. communis roots and stems, but the leaf Cd content was impacted by the degree of pollution. M. sativa had a significant effect on the Cd content of R. communis fruits, which was not affected by different pollution levels. The bioconcentration factor of R. communis was greatest, more than 1, under slight levels of pollution, and when pollution levels increased, the value decreased (Table 3). Table 3. Effects of different treatments on the Cd contents in different R. communis L. tissues. Group Cd (mg/kg) BCF Root Stem Leaf Fruit Rs 0.503a 1.343a 1.543a 0.173a 1.10 Rm 0.418a 0.66a 0.695b 0.1a 0.63 Rh 0.278a 0.558a 0.935b 0.345a 0.32 RMs 0.348a 0.453a 1.8a 0.488b 1.17 RMm 0.289a 0.513a 0.376b 0.469b 0.58 RMh 0.339a 0.568a 0.765b 0.193b 0.27 Rs: Ricinus communis L. + Slight level of pollution, Rm: Ricinus communis L. + Moderate level of pollution, Rh: Ricinus communis L. + High level of pollution, RMs: Ricinus communis L. + Medicago sativa L. + Slight level of pollution, RMm: Ricinus communis L. + Medicago sativa L. + Moderate level of pollution, and RMh: Ricinus communis L. + Medicago sativa L. + High level of pollution; different letters indicate significant differences (p < 0.05, one-way ANOVA, LSD test). Different treatments did not significantly affect the Zn content of R. communis roots and fruits, but different pollution levels affected the Zn content of stems. Furthermore, the Zn content of R. communis leaves was impacted by M. sativa. However, the bioconcentration factor of R. communis was less than 0.2, so the cumulative effect of Zn on R. communis remains unclear (Table 4). Table 4. Effects of different treatments on the Zn contents in different R. communis L. tissues. Group Zn (mg/kg) BCF Root Stem Leaf Fruit Rs 36.25a 28.71a 55.15a 29.073a 0.17 Rm 45.58a 29.805ab 44.105b 34.538a 0.12 Rh 37.225a 34.078b 41.058b 34.3a 0.12 RMs 43.395a 41.56a 53.78a 36.36a 0.14 RMm 42.683a 18.953ab 42.865b 34.415a 0.09 RMh 38.654a 23.243b 42.661b 31.841a 0.06 Rs: Ricinus communis L. + Slight level of pollution, Rm: Ricinus communis L. + Moderate level of pollution, Rh: Ricinus communis L. + High level of pollution, RMs: Ricinus communis L. + Medicago sativa L. + Slight level of pollution, RMm: Ricinus communis L. + Medicago sativa L. + Moderate level of pollution, and RMh: Ricinus communis L. + Medicago sativa L. + High level of pollution; different letters indicate significant differences (p < 0.05, one-way ANOVA, LSD test). 4. Discussion Phytoextraction efficiency is determined by two key factors: the biomass production and metal concentration of plants (Giordani et al., 2005). Plant biomass production is closely related to the height and stem circumference of plants, and in our experiment, M. sativa significantly increased the height and circumference of R. communis and promoted its growth. Other experiments have demonstrated that legumes can provide N, thus increasing the nitrogen content in the soil (Jensen and Hauggaard-Nielsen, 2003; Noble et al., 2008). Nitrogen is a raw material of biological proteins, nucleic acids and other nitrogen compounds, and when alfalfa was present, it provided a nitrogen source needed to produce growth hormones and synthesize nucleic acids that, in turn, promoted the growth of the castor bean. The height, stem circumference and biomass of R. communis was not significantly impacted by different levels of pollution, indicating that R. communis can tolerate heavy metals, and this is consistent with the results in the literature. Additionally, R. communis has been shown to be a metal-tolerant crop, with a high tolerance to Cd concentrations (Shi and Cai, 2009). Chlorophyll is the main photosynthetic pigment, and chlorophyll concentrations affect plant growth (Mani et al., 2015). Several studies have revealed that Cd can inhibit chlorophyll biosynthesis in plant leaves (Ali et al., 2017) and that a high total Zn content can cause chlorotic spots on plant leaves (Ma et al., 2015). In the present experiment, higher pollution levels had a greater impact on the chlorophyll content of R. communis. It has been reported that metals, if present at toxic levels, can interfere with normal enzyme functions in plants, and one of the plant processes most affected by Cd-toxicity is photosynthesis (Varun et al., 2017). M. sativa can alleviate heavy metal toxicity, and one possible pathway is that M. sativa provides N for the growth of R. communis. Because nitrogen is one of the essential nutrients for plant growth, it is part of all living cells, and it is also one of the important raw materials in some enzymes and is involved in enzymatic synthesis. Some of the enzymes that play an important role in alleviating heavy metal toxicity are peroxidase (PDX), catalase (CAT) and ascorbate peroxidase (APX) (Venkatachalam et al., 2017); M. sativa increased the content of these enzymes in R. communis and reduced the effects of heavy metals on plant photosynthesis. There are more than 350 species of oil crops in the world, and R. communis is among the most prominent (Bauddha et al., 2015). The oil content of R. communis fruits is important for investigating the effect of remediation. In our experiment, pollution levels significantly reduced the oil content of R. communis, which is consistent with the research of Olivares et al. (2013), but when M. sativa was present, the oil content of R. communis was differentially affected by different levels of pollution, indicating that M. sativa increased the oil content of R. communis and eased heavy metal poisoning. One possible explanation for this is that M. sativa is involved in enzymatic synthesis. The accumulation of cadmium and zinc in the ground portion of R. communis was far greater than that in the underground portion, and R. communis was also found to have extracted a number of heavy metals (Pandey, 2013). However, in the presence of M. sativa, R. communis roots had higher heavy metal accumulation levels. These results demonstrate that M. sativa can improve the accumulation of heavy metals in R. communis roots, and one possible mechanism is that some plant species exude H+ or low-molecular-weight organic acids into the soil, which can either directly or indirectly increase metal mobility by affecting microbial activity (Chen et al., 2003; Chiang et al., 2006; Duarte et al., 2007). Both cadmium and zinc exhibited the trend of shifting accumulation to plant leaves. Cd was mainly accumulated in the stems and leaves of R. communis, and Zn was mainly accumulated in the leaves, which influenced chlorophyll synthesis. The Cd concentration in R. communis roots was less than that in the stems because root tissue endodermis cells have a horizontal intercept (Seregin and Ivanov, 1997) that creates certain limitations. When the concentration of heavy metal ions was highest in the external environment, the horizontal intercept could be broken, and a large number of heavy metal ions is easier to transport into the ground. The BCF indicated that the uptake ability of a plant is important in assessing the feasibility of phytoextraction (McGrath and Zhao, 2003). Generally, a BCF value >1 is considered ideal for phytoextraction (Marques et al., 2009), and in our experiment, the BCF value in most treatments was less than 1, indicating that R. communis was not a zinc accumulator. Olivares et al. (2013) stated that castor bean does not accumulate metals even though the available concentration is high, which is consistent with the rest of our results. 5. Conclusions The presence of M. sativa affected the height and stem circumference of R. communis. It significantly increased the height and stem circumference and promoted the growth of R. communis. Higher heavy metal pollution levels had a greater impact on the chlorophyll content of R. communis, but M. sativa alleviated this effect. Pollution significantly reduced the oil content of R. communis fruits, but with the presence of M. sativa, the oil content was not affected by the different levels of contamination. The average accumulation of cadmium and zinc in R. communis with M. sativa was 1.14 and 2.19 times, respectively, the average accumulation in R. communis without M. sativa. Although the BCF value was less than 1 in most treatments, the total heavy metal accumulation was still very considerable since R. communis has such a large biomass. Acknowledgements This research was supported by the National Key R & D Program of China (Project No. 2016YFA0601003), the Program for Innovative Research Team in University (No. IRT13078) and the Grant-in-Aid for Scientific Research of the Japan Society for the Promotion of Science (No. 23405049). References Ahmadpour et al., 2012 P. 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