3.1. The concentrations of heavy metals in rapeseed samples grown at different temperatures
Figures 3, 4 and 5 show the concentrations of heavy metals in rapeseed samples grown at different temperatures (22.5, 22.9, 23.7, and 24.6°C) at the vegetative, reproductive, and maturity stages. At the vegetative stage, no significant variations (p > 0.05) were found in the As, Pb, Cd, and Cu concentrations in rapeseed plants grown with different soil temperature. However, the Zn concentration in rapeseed plants showed significant differences with different soil temperatures. The Zn concentrations in rapeseed were 136.93 ± 21.85, 167.79 ± 0.09, 182.51 ± 26.79, and 257.72 ± 34.16 mg·kg-1 at 22.4, 22.9, 23.7, and 24.6°C, respectively. At the reproductive stage, the concentrations of all heavy metals in the total biomass were highest at the highest temperature (24.6°C). This tendency was more evident in the roots than in the shoots. In particular, the total As concentration was significantly increased by 75.5% at 24.6°C compared to that detected at ambient temperature (22.5°C). At the maturity stage, the Cu, Zn, and Cd in total biomass were lowest at ambient temperature. The Zn concentration in the shoots and total biomass showed significant differences with different temperatures. Overall, the influence of temperature varied depending on the heavy metal and the growth stage. However, the heat treatment enhanced the heavy metal concentrations in rapeseed, particularly that of Zn.
The partial correlation coefficients of the heavy metal concentrations in rapeseed and the soil temperature controlling the growth stage are listed in Table 2. The order of partial correlation coefficients was Zn (0.50) > Cd (0.21) > Cu (0.19) > As (0.15) > Pb (0.13). All heavy metals showed positive correlations, but only Zn showed a significant moderate positive correlation with the soil temperatures (r = 0.50, p < 0.01). These data suggest that an increase in soil temperature may promote the soil-to-plant transfer of metals, especially Zn, by facilitating the capture of metals. Table 3 shows Pearson correlation coefficients between the heavy metal concentrations in rapeseed plants and soil temperatures. The concentration of Zn in rapeseed during the vegetative stage correlated positively with the soil temperature (r = 0.77, p < 0.01). In addition, at all growth stages, the Zn and Cd concentrations in rapeseed showed strong positive relationships, with correlation coefficients of 0.78, 0.85, and 0.76, because they have similar chemical and physical behaviors (Kubiera et al., 2019). Although the Cd concentration in rapeseed did not significantly correlate with the temperature in this experiment, the possibility remains that an increase in soil temperature may affect Cd accumulation in rapeseed tissues if the soil is heavily contaminated with Cd. Recent findings related to metal transporter (Duo et al., 2018) showed that rapeseed has some Zn/Cd transporters such as NRAMP, ZIP, and HMAP (Krämer et al., 2007).
Table 2
Partial correlation coefficients of the concentration of heavy metals in rapeseed and soil temperature after controlling time points
Heavy metal | Coefficients | p-value | statistic | n |
---|
Zn | 0.501 | 0.002 | 3.32 | 36 |
Cd | 0.206 | 0.23 | 1.21 |
Cu | 0.188 | 0.27 | 1.10 |
As | 0.148 | 0.39 | 0.86 |
Pb | 0.129 | 0.45 | 0.75 |
Table 3
Pearson correlation coefficients between the heavy metal concentrations in rapeseed plants and soil temperatures
Growth stage (Time point) | Heavy metal | Temperature | Zn | Cd | Cu | As | Pb |
---|
Vegetative (5 weeks) | Zn | 0.77** | 1 | | | | |
Cd | 0.45 | 0.78** | 1 | | | |
Cu | 0.29 | 0.41 | 0.58. | 1 | | |
As | 0.23 | -0.18 | 0.02 | 0.32 | 1 | |
Pb | 0.19 | -0.14 | 0.12 | 0.37 | 0.96 | 1 |
Reproductive (10 weeks) | Zn | 0.4 | 1 | | | | |
Cd | 0.13 | 0.85** | 1 | | | |
Cu | 0.4 | 0.83** | 0.66* | 1 | | |
As | 0.61. | 0.71* | 0.43 | 0.72* | 1 | |
Pb | 0.43 | 0.91*** | 0.69* | 0.92*** | 0.86** | 1 |
Maturity (15 weeks) | Zn | 0.49 | 1 | | | | |
Cd | 0.35 | 0.76** | 1 | | | |
Cu | -0.04 | 0.47 | 0.47 | 1 | | |
As | -0.45 | 0.23 | 0.26 | 0.6. | 1 | |
Pb | -0.34 | 0.37 | 0.26 | 0.69* | 0.95*** | 1 |
***p < 0.001; **p < 0.01; *p < 0.05; .p < 0.1 |
According to Lynch & Steponkus (1987), an increased temperature generally increases the number of active sites on the surface of roots and modifies the lipid contents of the plasma membrane, which enhances both passive and active metal flow through the membrane (Fritioff et al., 2005). Fritioff (2005) found that the effects of warming on heavy metal accumulation in submerged plants, such as Elodea canadensis and Potamogeton natans L., and observed that the Cu, Zn, and Cd concentrations in the plant tissues increased with elevated temperatures in both species. Li et al., (2012) observed that temperatures elevations of + 1, +2, and + 3°C above ambient temperature increased the Cu, Zn, and Fe concentrations in leaf potato plants by 25, 27, and 24%, respectively. In addition, increasing temperatures resulted in higher rates of metabolism and protein synthesis (Marschner, 2011; Orcutt, D. M., & Nilsen, 2000). These changes could lead to enhanced metal uptake at additional metal-uptake sites in plants. Zinc is an essential micronutrient for plants that activates enzymes involved in protein synthesis (Castillo-González et al., 2018). Therefore, in this study, the enhanced enzymatic activity due to an elevated temperature would have boosted the absorption of Zn more rapidly and significantly than other heavy metals in rapeseed.
3.2. The total and bioavailable concentrations of heavy metals in soil samples at different temperatures
The total and bioavailable concentrations of heavy metals in the soil are listed in Table 4. Regardless of soil temperatures, the average concentrations of all heavy metals in the soil samples at 5 and 10 weeks were slightly lower than the initial values. However, the concentrations of heavy metals in soil at 15 weeks were higher than those in the soil samples at 10 weeks regardless of temperatures and heavy metal. The Cu and Zn concentrations were similar or slightly higher than the initial values. The total and bioavailable concentrations of heavy metals in the soil did not significantly increase or decrease with changes in the soil temperature. In addition, the values of the correlation coefficients did not show any relationship between soil heavy metal concentrations and soil temperatures. In general, soil warming can alter how soluble metal ions are released into soil solution through the decomposition of SOM, lysis of microbial cells, and the destruction of soil aggregates (Rajkumar et al., 2013). However, in this study, significant changes in soil heavy metal concentrations were not observed in accordance with temperature differences because the experimental period was short and the temperature gradient was not large. Our results imply that the transport of heavy metals from most soils to plants with increasing soil temperature was influenced by plant mechanisms, rather than soil-related processes (Cornu et al., 2016).
Table 4
The total and bioavailable concentrations of heavy metals in soil samples at different temperatures (22.5, 22.9, 23.7, and 24.6°C).
Heavy metal | Time point | Total concentration of heavy metals in soil (mg kg− 1) | | Bioavailable concentration of heavy metals in soil (mg kg− 1) |
22.5°C | 22.9°C | 23.6°C | 24.7°C | 22.5°C | 22.9°C | 23.6°C | 24.7°C |
Zn | 5weeks | 455.6 ± 11.6 | 447.83 ± 15.4 | 417.23 ± 16.5 | 458.3 ± 13.3 | | 106.16 ± 2.01 | 102.27 ± 2.02 | 91.45 ± 1.5 | 104.24 ± 2.27 |
10weeks | 429.37 ± 6.3 | 448.27 ± 16.0 | 452.23 ± 3.6 | 413.77 ± 14.3 | 104.71 ± 2.6 | 98.11 ± 5.75 | 88.83 ± 6.75 | 90.64 ± 0.77 |
15weeks | 483.87 ± 20.8 | 501.07 ± 8.1 | 512.07 ± 9.7 | 461 ± 15.7 | 115.07 ± 0.78 | 117.97 ± 3.43 | 119.97 ± 2.25 | 121.46 ± 2.77 |
Cd | 5weeks | 2.13 ± 0.05 | 1.97 ± 0.05 | 1.83 ± 0.11 | 2.1 ± 0.05 | | 1.46 ± 0.03 | 1.4 ± 0.04 | 1.21 ± 0.02 | 1.41 ± 0.04 |
10weeks | 2.37 ± 0.07 | 2.3 ± 0.08 | 2.47 ± 0.05 | 2.27 ± 0.1 | 1.44 ± 0.04 | 1.34 ± 0.07 | 1.25 ± 0.1 | 1.25 ± 0.02 |
15weeks | 2.67 ± 0.14 | 2.73 ± 0.05 | 2.73 ± 0.14 | 2.53 ± 0.14 | 1.69 ± 0.02 | 1.72 ± 0.04 | 1.73 ± 0.03 | 1.77 ± 0.04 |
Cu | 5weeks | 51.37 ± 0.11 | 46.7 ± 1.56 | 43.63 ± 0.38 | 51.67 ± 2.06 | | 14.21 ± 0.18 | 14 ± 0.24 | 12.91 ± 0.22 | 15.51 ± 0.51 |
10weeks | 44.4 ± 1.11 | 49.2 ± 2.07 | 49.57 ± 1.16 | 42.7 ± 1.41 | 13.66 ± 0.35 | 13.12 ± 0.8 | 13.04 ± 0.84 | 12.66 ± 0.23 |
15weeks | 57.13 ± 3.81 | 60.2 ± 0.62 | 57.13 ± 3.57 | 51.6 ± 1.41 | 14.95 ± 0.17 | 16.24 ± 0.57 | 15.98 ± 0.41 | 15.22 ± 0.17 |
As | 5weeks | 69.87 ± 1.26 | 67.5 ± 1.82 | 59.33 ± 0.48 | 68.93 ± 1.46 | | 2.25 ± 0.01 | 2.17 ± 0.01 | 2.07 ± 0.03 | 2.18 ± 0.02 |
10weeks | 61.87 ± 1.16 | 65.4 ± 2.13 | 67.67 ± 0.79 | 62.03 ± 1.95 | 2.07 ± 0.01 | 2.01 ± 0.02 | 1.96 ± 0.03 | 2.01 ± 0.02 |
15weeks | 73.93 ± 2.14 | 78.53 ± 2.04 | 76.13 ± 4.46 | 72.87 ± 2.27 | 2.43 ± 0.03 | 2.36 ± 0.02 | 2.33 ± 0.03 | 2.43 ± 0.05 |
Pb | 5weeks | 833.33 ± 16.6 | 758.03 ± 12.3 | 671.13 ± 6.7 | 793.9 ± 49.0 | | 20.61 ± 0.46 | 19.17 ± 0.39 | 17.38 ± 0.37 | 19.67 ± 0.6 |
10weeks | 745.4 ± 7.8 | 806.03 ± 8.8 | 836.77 ± 20.9 | 747.13 ± 31.1 | 20.7 ± 0.53 | 19 ± 0.9 | 17.42 ± 1.03 | 18.04 ± 0.23 |
15weeks | 835.73 ± 17.6 | 855.27 ± 10.3 | 859.8 ± 43.7 | 824.27 ± 23.0 | 14.67 ± 1.1 | 15.28 ± 0.8 | 15.2 ± 0.61 | 15.77 ± 0.84 |
3.3. Changes in soil geochemical properties at different temperatures
The values of the soil properties, including the pH, EC, OM, and CEC, at different temperatures are shown in Table 5. The Soil pH decreased with time in all temperature treatments, but the differences of value according to temperature were insignificant, less than 0.1. The amount of OM in the soil increased noticeably by 20% at maturity (15 weeks) relative to that at the reproductive stage (10 weeks) under all temperature treatments. It is probably because the rapeseed leaves fell into the soil and that the root volume of the rapeseed plants in the soil increased during maturity. The values of CEC showed a similar tendency compared to the SOM content. In general, CEC increases with SOM content because humic substances usually contain several functional groups that can retain cations (Biswas et al., 2018). Overall, owing to the complex process and buffering effect of the soil, no significant differences in absolute values of the soil geochemical properties were found according to the temperature. However, the partial correlation coefficient results after controlling time points showed that the soil pH correlated positively (r = 0.49, p < 0.01) with the soil temperature, whereas the CEC correlated negatively (r = -0.55, p < 0.001) with the soil temperature (Table 5). In general, soil geochemical properties can change during heating treatment as a consequence of increased soil respiration and microbial and enzymatic activities (Rajkumar et al., 2013). The results of a previous study showed that a winter temperature rise resulted in a significant increase in the soil pH; a temperature increase of 0.5°C-2.0°C led to an increase in the soil pH by 0.42–0.67 units (Guoju et al., 2012). However, Ge et al. (2016) found the opposite results: warming gradually decreased soil pore water pH values, increased soluble Cd and Cu concentrations, and further influenced the accumulation of metals in rice plants. In the case of CEC, although we did not observe SOM changes in this study according to temperature, previous findings (Antoniadis & Alloway, 2001; Cornu et al., 2016; Haghiri, 1974) showed that OM degradation in the soil accelerated when the soil temperature increased, resulting in decreased CEC. The soil CEC is an indicator of the ability to capture cations and immobilize heavy metals (Cui et al., 2021). The results of this study show that a reduced CEC led to the release of metals bound to soil particles, leading to increased heavy metals concentrations in plants, in agreements with previous findings (Antoniadis & Alloway, 2001). Because soil has extensive properties depending on the region and vegetation, various studies (Crowther et al., 2016; Guoju et al., 2012; Smith et al., 2002; Wang et al., 2021) have been conducted to determine how soil temperatures change soil properties, including the soil pH, SOM, soil nutrients, and humidity.
Table 5
Geochemical properties in the soil samples at different temperatures (22.5, 22.9, 23.7, and 24.6°C) and partial correlation coefficients of the geochemical properties and soil temperature after controlling time points
Soil properties | Time points | Average soil temperature | Coefficient |
---|
22.5°C | 22.9°C | 23.6°C | 24.7°C |
---|
pH (1:5) | 5 weeks | 6.71 ± 0.008 | 6.69 ± 0.037 | 6.77 ± 0 | 6.78 ± 0.002 | 0.49** |
10 weeks | 6.52 ± 0.022 | 6.61 ± 0.007 | 6.63 ± 0.006 | 6.63 ± 0.020 |
15 weeks | 6.60 ± 0.019 | 6.54 ± 0.004 | 6.52 ± 0.029 | 6.59 ± 0.013 |
EC (ds/m) | 5 weeks | 0.38 ± 0.023 | 0.33 ± 0.009 | 0.35 ± 0.011 | 0.36 ± 0.016 | -0.42* |
10 weeks | 0.58 ± 0.055 | 0.38 ± 0.024 | 0.32 ± 0.001 | 0.45 ± 0.023 |
15 weeks | 0.51 ± 0.004 | 0.51 ± 0.030 | 0.37 ± 0.007 | 0.41 ± 0.023 |
OM (%) | 5 weeks | 3.83 | 3.57 | 3.37 | 3.6 | -0.05 |
10 weeks | 3.46 | 3.71 | 3.48 | 3.35 |
15 weeks | 4.04 | 4.18 | 4.52 | 4.32 |
CEC (meq/100g) | 5 weeks | 13.4 ± 0.28 | 12.3 ± 0.22 | 11.4 ± 0.59 | 11.8 ± 0.12 | -0.56*** |
10 weeks | 12.8 ± 0.13 | 12.5 ± 0.18 | 11.7 ± 0.05 | 11.7 ± 0.26 |
15 weeks | 13.3 ± 0.28 | 14.1 ± 0.52 | 13.9 ± 0.28 | 13.3 ± 0.54 |
***p < 0.001; **p < 0.01; *p < 0.05; .p < 0.1 |
3.4. BCF and TF values of rapeseed samples grown at different temperatures
The BCF is a quantifiable indicator of plant contamination that has commonly been used to estimate the transfer of toxic elements from soil to plants (Chang et al., 2014; Melgar et al., 2009). The BCF is calculated as the ratio of the concentration of an element in a plant to that in the soil. In this study, BCF values (Fig. 6) showed a similar trend to heavy metal accumulation in rapeseed samples described in the section titled, “The total and bioavailable concentrations of heavy metals in soil samples at different temperatures.” At the reproductive stage, all heavy metals showed the highest values at the highest temperature. The BCF values of the other heavy metals in the maturity stage, except for As, were lowest at the ambient temperature. The average BCF values for all growth stages and temperatures were in the order Cd > Zn > Cu > As > Pb. Our results are consistent with the results of several studies showing that the BCF values of Cd and Zn were greater than 1 and that rapeseeds accumulate large amounts of Cd and Zn. Many studies have been conducted on the potential of rapeseed to act as a hyper-accumulator for Cd and Zn (Duo et al., 2018; Grispen et al., 2006; Marchiol et al., 2004; Rosca et al., 2021). The TF values were determined to evaluate the capacity of plants to mobilize heavy metals from the roots to the aerial parts (Clemens & Ma, 2016; Wan et al., 2015; Yu et al., 2012). At the reproductive stage, the TF values of most heavy metals, except for As, were lowest at the highest temperature, because the accumulation of heavy metals in roots was the highest at 24.6°C (Fig. 7). In general, to absorb trace elements, metals must be captured by root cells after mobilization (Clemens & Ma, 2016). Because elevated temperatures increase the uptake of micronutrients in the roots (Miyasaka & Grunes, 1997), the TF values decreased during the reproductive stage, which requires a large amount of nutrients (Edwards & Hertel, 2011). However, at the maturity stage, the TF values of all heavy metals were highest at the highest temperature. It was previously presumed that the maximum nutrient uptake declined after flowering (Malhi et al., 2007), considering that only the transport process in the plant tissue affected the TF factors at the maturity stage. Higher temperatures increased the vapor pressure deficit of the environment surrounding the leaves, thereby increasing the rate of transpiration (Trenberth et al., 2005). As a result, increased transpiration caused heavy metals to be unloaded from the xylem and phloem and delivered to various aboveground organs (Yamaji & Ma, 2014). Those results are in agreement with the results of other several studies (Cornu et al., 2016; Farhat et al., 2021; Ge et al., 2016; Li et al., 2012), which revealed a positive relationship between soil temperatures and the TF values of Zn, Cd, and Pb at the maturity stage. These data suggest that future elevated temperatures could induce more heavy metal uptake through the transport of heavy metals to the aerial parts of plants, such as leaves, grains, and fruits. In this study, the order of the average TF values for all temperatures was Cd > Zn > Cu > As > Pb during the reproductive stage and Zn > Cd > Cu > As > Pb during the maturity stage. The TF values for Zn, Cd, and Cu were greater than 1, and the TF values for Pb and As were less than 1. Previous data demonstrated that heavy metals were transported to aerial parts of plants to a limited extent and that plants could expel the toxicant (Olowoyo et al., 2010). For most toxic metals such as As and Pb, the rate of metal translocation from the roots to shoots is much lower than the rate of uptake of essential elements including Zn and Cu (Meagher, 2000). Moreover, our current results are consistent with those of several studies on the mobility and transport of heavy metals, where Pb exhibits low mobility, and Cd and Zn exhibit high mobility (Berlin, 1986; Chen et al., 2016; Violante et al., 2003; Yu et al., 2012).