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Article

Effects of Different Carbon Types on the Growth and Chromium Accumulation of Peach Trees under Chromium Stress

by
Huaifeng Gao
,
Xiaoqing Yang
,
Nana Wang
,
Maoxiang Sun
,
Yuansong Xiao
and
Futian Peng
*
State Key Laboratory of Crop Biology, College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an 271018, China
*
Author to whom correspondence should be addressed.
Agronomy 2022, 12(11), 2814; https://doi.org/10.3390/agronomy12112814
Submission received: 12 October 2022 / Revised: 4 November 2022 / Accepted: 10 November 2022 / Published: 11 November 2022
(This article belongs to the Special Issue Heavy Metal Pollution of Agricultural Soils: Treatment and Restoration)
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Abstract

:
Heavy metal pollution in agricultural soil is a serious problem, which threatens the environment and human safety. In this study, the effects of biochar (BC), activated carbon (AC), and nanocarbon (NC) on the growth of peach trees under chromium (Cr) stress were investigated through pot experiments. The experimental results showed that under Cr stress, BC, AC, and NC could increase the soil nutrient content and enhance the soil enzyme activity. Moreover, all carbon forms promoted the conversion of Cr speciation; decreased the content of exchangeable (EXE), carbonate-bound (CARB), and iron–manganese-oxide-bound (FeMnO) Cr in the soil; increased the organic-bound (Org) and precipitated (Pre) Cr content; and reduced Cr availability. After BC, AC, and NC treatment, the content of Org-Cr in the soil increased by 86.05%, 72.97%, and 65.02%; the content of EXE-Cr decreased by 75.30%, 75.33%, and 73.10% compared with the control under severe Cr treatment, respectively. Moreover, the accumulation of Cr in plants decreased by 29.70%, 22.07%, and 20.52%, respectively. At the same time, these three carbons reduced the accumulation of Cr in various parts of the peach tree, alleviated the oxidative damage caused by Cr stress, effectively protected the photosystem of the leaves, improved the photosynthetic capacity, and promoted the growth of the peach tree. Compared with the control, the dry matter accumulation increased by 20.81%, 9.54%, and 6.95% with BC, AC, and NC treatment under severe Cr treatment. Therefore, BC, AC, and NC can all effectively alleviate soil Cr toxicity, and BC has the best effect, which can be popularized in production.

1. Introduction

With the rapid development of industry and the acceleration of urbanization, an increasing number of industrial pollutants are discharged into the environment, and the problem of heavy metal pollution is particularly serious [1,2,3]. Compared with other types of pollutants, the particularity of heavy metal pollution is that heavy metal pollutants have poor mobility and nondegradability, so they easily accumulate in soil in various forms. Heavy metal pollutants move freely through various media, leading to persistent pollution in the environment. While seriously endangering the ecosystem, heavy metal pollution also poses a serious threat to human life and health [4,5]. Problems such as soil quality degradation or crop yield and quality decline caused by excessive accumulation of heavy metals in soil have posed a serious threat to human health [6,7]. There have been frequent reports of heavy metal contamination of soil and water sources around the world [8]. Therefore, scientifically and effectively mitigating the harm of polluted soil to the environment and human beings is increasingly important.
Cr is widely found in nature, and trace amounts of Cr are contained in the atmosphere, water, and soil. The content of Cr in plants is mainly affected by the content of Cr in soil; the general mass fraction of Cr in plants is below 0.001–0.005%, and green plant parts have the highest Cr content [9]. In the natural environment, Cr mainly exists in two stable valence states, namely, Cr(III) and Cr(VI). The solubility of Cr(III) in soil is low (<10–5 M) over a wide pH range, so its mobility is poor, and its toxicity to organisms is relatively low [10,11]. However, Cr(VI) mainly exists in the form of ions in the soil and has high mobility and bioavailability. The toxicity of Cr(VI) is 100 times greater than that of Cr(III), and it has a strong carcinogenic effect on organisms. The migration and transformation of Cr in the environment is very active and is mainly determined by physical and chemical processes, such as redox reactions, precipitation dissolution, adsorption, and desorption [12,13]. The forms of Cr in soil are divided into the water-soluble state, ion-exchange state, carbonate-bound state, iron–manganese-oxide-bound state, organic sulfide-bound state, and residue state. Among them, the water-soluble and ion-exchange states migrate easily and are easily bioavailable [14,15,16].
Cr is an important trace element for plants, and low concentrations of Cr can stimulate the growth and development of crops. However, excess Cr can have adverse effects, such as stunted plant development and decreased yield [17,18]. Cr induces phytotoxicity by interfering with plant growth, nutrient uptake, and photosynthesis, causing lipid peroxidation and altering antioxidant activity [19,20]. Excess Cr damages plant roots, reduces the activity of reactive enzymes, and causes chlorosis or even necrosis of plant tissues [21,22,23]. Excessive Cr can cause mosaic disease, cucumber cancer, spinach tumors, and pineapple tumors and inhibit the growth of rice, corn, cotton, rape, radish, and other crops. Cr can affect the activities of soil enzymes and micro-organisms, which increases the safety risk of soil ecology [24]. Cr is toxic to micro-organisms mainly by destroying the active structure of certain enzymes in micro-organisms or enriching them to a certain concentration [25]. As the concentration of Cr in the soil increases, the growth and metabolism of micro-organisms are restricted, which eventually leads to a decrease in the number of micro-organisms, such as bacteria and actinomycetes, in the soil and a decrease in enzyme activity [26]. In addition, in the process of stress cell death, Cr is also accompanied by a significant increase in intracellular reactive oxygen species, calcium ions, and nitric oxide and a significant decrease in membrane potential [27,28,29]. The accumulation of Cr in the human body can cause the precipitation of certain proteins in the blood, leading to anemia and neuritis, and severe poisoning can induce lung cancer and even death [30].
There are usually two remediation mechanisms for soil Cr pollution from a soil–plant transfer point of view. One mechanism is to reduce the migration ability and bioavailability of Cr(VI) in the environment by changing the existing form of Cr(VI) in the soil, and the other mechanism is to remove Cr from the contaminated soil [31,32,33]. Adsorption has become the main method for removing heavy metals due to its simple operation and high removal efficiency. Carbon materials have great potential in the remediation of heavy-metal-contaminated soil and water sources because of their wide sources, low cost, and no secondary pollution [34,35]. One study found that adding green manure, farmyard manure, crop straw, BC, coal ash, and lime can effectively alleviate Cr poisoning [36,37]. AC is a type of microcrystalline carbon composed of carbonaceous materials with a black appearance, developed internal voids, and large specific surface area and is widely used in the treatment of pollutants [38]. Nanomaterials have the characteristics of quantum effects, surface effects, and small-size effects. NC has a very large surface area and strong surface activity, and it has been confirmed that it can combine with Cu(II) through coprecipitation and other processes, thereby increasing the adsorption of Cu(II) [39]. BC has a large specific surface area, high pH value, and cation exchange capacity, which can improve the electrostatic adsorption capacity of heavy metals in soil [40,41]. In addition, the surface of BC is rich in oxygen-containing functional groups (such as carboxyl, phenol, hydroxyl, carbonyl, and quinone), which can increase the adsorption capacity of soil for heavy metals and reduce the mobility of heavy metals, thereby reducing toxicity [42].
Cr is an important environmental pollution element. When the content of Cr in the soil is too high, it can pollute the soil, affect the growth and development of the roots and leaves of crops, and accumulate in the edible parts of crops, causing harm to human health. China is the world’s largest producer of peach (Prunus persica L.), and some improper measures have increased the index of orchard soil contaminated by Cr. This study investigated the effects of AC, BC, and NC on the growth and Cr absorption of peach trees under the treatment of moderate and high concentrations of exogenous Cr pollution through pot experiments to provide a scientific basis for reducing the risk of Cr pollution in peach trees.

2. Materials and Methods

2.1. Plant Materials and Treatments

The experiment was performed at the experimental station of Shandong Agricultural University, and the varieties tested were 2-year-old ‘Luxing/Maotao’ grafted seedlings. The potting soil was peach orchard soil, and the main physical and chemical properties of the soil were: pH of 6.5, available nitrogen (inorganic nitrogen: ammonium nitrogen, nitrate nitrogen, and easily hydrolyzed organic nitrogen) content of 48.53 mg/kg, Olsen phosphorus (soluble inorganic phosphorus compounds, adsorbed phosphorus) content of 31.93 mg/kg, available potassium (replaceable potassium on the surface of the soil colloid and potassium ions in the soil solution) content of 84.72 mg/kg, organic matter content of 12.68 mg/kg, and a soil total Cr content of 12.13 mg/kg. The top diameter of the flowerpot was 32 cm, the bottom diameter was 22 m, and the height was 22 cm, and each pot was filled with 10 kg of soil. The Cr reagents tested were analytically pure K2Cr7O7, BC (carbonized rice husk, Anhui Xuancheng Jiale Rice Co., Ltd. (Anhui, China); after the rice husk is purified with HR acid, it is calcined at 600 °C); powder-free AC (Tianjin Kaitong Chemical Reagent Co., Ltd. (Tianjin, China); coaly activated carbon); NC (Beijing Niaisi New Materials Co., Ltd. (Beijing, China); particle size 50 nm, purity 99.9%).
The test period was from March to October 2020, and three concentrations of Cr were added to 0, 100, and 150 mg/kg (represented as Cr0, Cr100, and Cr150, respectively). According to the nutrient requirements of potted crops, the doses of nitrogen, phosphorus, and potassium for base fertilizers were 0.4 g N, 0.2 g P2O5, and 0.4 g K2O per kg of soil, respectively, which were evenly mixed into the soil. Under different Cr concentration treatments, BC, AC, and NC were added, and the blank treatment was used as a control. The application amount of BC and AC was 0.8% of the soil weight, and the NC was 3 mL. The experiment used a completely randomized block design with 12 treatments in total, with 6 replicates for each treatment. The soil, fertilizer, and reagents (after dissolving in 2 kg water, sprayed evenly) were mixed well, placed in pots, and equilibrated for two weeks. Two weeks later, the grafted seedlings of peach trees with basically the same growth potential and no pests or diseases were planted in the pots, one plant per pot, planted under natural conditions. Normal management after planting involved regular watering to maintain 60% of the field water capacity. During the period of vigorous growth of peach trees from June to September, various physiological indicators were measured. On 15 September, whole peach trees were sampled, and the plants were parsed, washed, and dried. The dry weight of the aboveground and underground parts was measured, and the Cr content in each part was measured.

2.2. Determination of Plant Physiological Indicators

The growth of shoots (cm) was measured with a tape measure, and 3 shoots were selected from each peach sapling to measure one repetition, which was repeated 6 times. A Vernier calliper was used to measure the trunk diameter (mm) of peach trees at a distance of 5 cm from the ground in each treatment, which was repeated 6 times for each plant. Each tree was marked with 6 leaves in the middle of the shoots, and the net photosynthetic rate of the leaves was determined, which was repeated 6 times. The photosynthetic rate was measured with a CIRAS-3 photosynthesis instrument produced by PP Systems (Hitchin, UK). The chlorophyll content was determined by spectrophotometry. The collected peach tree leaves were washed, cleaned, and cut into pieces. The veins were removed and mixed well, and then, the quartz sand, calcium carbonate, and 95% ethanol were added for grinding and filtering. The absorbance was measured at 649 nm and 663 nm, and the content of each photosynthetic pigment was calculated. Chlorophyll fluorescence kinetic parameters were measured by an FMS-2 portable modulation fluorometer produced by Hansatech (Pentney, UK), and the chlorophyll fluorescence induction curve and its parameters were determined according to the method of Georgia [43].

2.3. Antioxidant Enzyme Activity Assay

The activity of catalase (CAT) was measured by the UV absorption method; the activity of peroxidase (POD) was measured by the guaiacol chromogenic method; and the activity of superoxide dismutase (SOD) was measured by the nitroblue tetrazolium photoreduction method. The content of malondialdehyde (MDA) was determined by the thiobarbituric acid (TBA) colorimetric method.

2.4. Soil Enzyme Activity Assay

Using the quarter sampling method, a soil drill was used for sampling at 5–10 cm from the main trunk; the sampling depth was 0–20 cm, and 3 trees were taken for each treatment. The retrieved soil samples were naturally air-dried and then passed through a 1 mm sieve after grinding. The experiment was carried out according to Guan’s method [44]. Soil invertase activity was determined by 3, 5-dinitrosalicylic acid colorimetry; soil urease was determined by sodium phenolate colorimetry; soil acid phosphatase activity was determined by disodium phenyl phosphate colorimetry; and soil hydrogen peroxide enzyme activity was determined by potassium permanganate titration.

2.5. Determination of Soil Physical and Chemical Properties

The soil samples were taken following the quartering method with an earth drill and then passed through a 0.25 mm sieve after natural air-drying [45]. The basic physical and chemical properties of the soil were determined by conventional analytical methods, and soil organic matter was determined by the potassium dichromate volumetric method; alkaline hydrolysis nitrogen was determined by the alkaline hydrolysis diffusion method; the available phosphorus was determined by the 0.5 mol/L NaHCO3-molybdenum antimony resistance colorimetric method; the available potassium was extracted with NH4OAc-flame photometry; and soil pH was determined by the pH of the soil water extract.

2.6. Determination of Heavy Metal Content in Soil

After removing the foreign objects from the collected soil samples, approximately 1 kg was kept according to the quartering method and then passed through a 0.25 mm sieve after natural air-drying. A total of 0.2 g of soil sample (accurate to 0.0001) was accurately weighed, placed in a polytetrafluoroethylene digestion tube, added to 3 mL of 65% HNO3 and 3 mL of 40% HF, and placed into a microwave digestion apparatus (Mars 6, CEM, North Carolina, NC, USA) to perform high-temperature digestion. After digestion, the solution was pale yellow-green, and the volume was brought up to 50 mL with ultrapure water. The content of heavy metals in the digestion solution was determined by an inductively coupled plasma mass spectrometer (Nex ION 300X, Per Kin Elmer, Waltham, MA, USA) [46].

2.7. Determination of Heavy Metal Cr Speciation in Soil

A 5 g soil sample was taken for continuous extraction, and the speciation of metallic Cr was determined by atomic absorption spectrophotometry. The selection and sequence of extractants were as follows: (1) for EXE-Cr, 1 mol/L NH4Ac solution was utilized; (2) for CARB-Cr, 0.1 mol/L EDTA (pH 6.5) solution was used; (3) for FeMnO-Cr, 25 mL of 0.1 mol/L NH2OH·HCl solution was added and shaken for 2 h; a total of 25 mL of 0.1 mol/L NH4Ac solution was added to the mixture and equilibrated for 2 h; (4) for Pre-Cr, 2 mol/L HCl solution was used; (5) for Org-Cr, 10% H2O2-2 mol/L HCl solution was utilized; and (6) Res-Cr was calculated by subtracting the contents of the above five speciations of Cr from the total Cr content in the soil. The soil and extract ratios were both 1:10. For each extraction, the residue after washing in the previous step was added to the extraction solution, shaken for 2 h, equilibrated for 2 h, and centrifuged (4000 rpm, 20 min), and the supernatant was analyzed for various forms of Cr content [47].

2.8. Analysis of Plants and Determination of the Total Cr Content

After sample collection, the samples were rinsed with water first and then with ultrapure water. The plants were then decomposed into fine roots (diameter ≤ 2 mm), thick roots (diameter ≥ 2 mm), trunk xylem, trunk phloem, new branch xylem, new branch phloem, and leaves. The samples were fixed at 105 °C for 0.5 h, dried at 80 °C to constant weight. The dried samples were pulverized and passed through a 0.25 mm sieve for later use. We accurately weighed 0.30 g of the sample (accurate to 0.0001), added 5 mL of the HNO3-H2O2 mixed solution, and performed high-temperature digestion with a microwave digestion apparatus. The other steps were the same as those for the determination of heavy metals in the soil.

2.9. Statistical Analysis

The biological and biochemical data are presented as means ± standard errors (SEs). The significance of the differences between samples was assessed by Duncan’s multiple range tests using SPSS version 20.0.

3. Results

3.1. Investigation of Cr Content in Orchard Soils in Different Regions of China

A comparison of 112 soil samples from six major peach-producing areas in China was compiled (Table S1). The number of sampling points in each region is as follows: 7 in northeast China; 23 in north China; 41 in east China; 15 in central China; 20 in northwest China; and 6 in southwest China. The Cr content in the orchard soil was measured, and it was found that the average soil Cr content was 49.25 mg/kg, and the orchard soil Cr content in the southwestern region was higher than that in other regions. The level of heavy metals in the soil of each peach-producing area was evaluated using the secondary standard in China’s ‘Evaluation Standard for Heavy Metal Pollution in Soil’. The average Cr pollution index of the 112 soil samples collected was 0.25; all pollution indices were less than 1, and the Cr content of the samples did not exceed the standard.

3.2. Effects of Different Carbons on Soil Physicochemical Properties under Cr Stress

Exogenous Cr application changed the soil physicochemical properties, while BC, AC, and NC could reduce the adverse effects of Cr on soil (Table 1). As the Cr concentration in the soil increased, the pH of the soil increased, which was alleviated by the BC and AC treatments. BC, AC, and NC application increased the organic matter content of the soil, and the increase in organic matter content could buffer soil pH changes and alleviate the effect of Cr on soil pH. Compared with the control treatment, exogenous Cr decreased the content of soil Olsen-P and available N but had no effect on the content of available K. BC, AC, and NC could alleviate the decrease in soil Olsen-P and available N content and increase the soil available K content under Cr stress, and BC had the best effect. Compared with CK, under moderate Cr stress, the contents of Olsen-P, available K, and available N increased by 39%, 12%, and 10%, respectively, and they increased by 43.31%, 14%, and 13%, respectively, under severe Cr stress. These results indicated that NC, AC, and NC could all improve the physicochemical properties of soil under Cr stress, with BC being the best.

3.3. Effects of Different Carbon Types on Soil Enzyme Activities under Cr Stress

Exogenous Cr application significantly affected soil enzyme activities. As shown in Figure 1A–D, the four soil enzyme activities decreased with increasing Cr concentration. In the absence of exogenous Cr contamination, BC, AC, and NC had little effect on the four soil enzymes. Under moderate Cr stress, BC had the most obvious enhancement effect on soil invertase, urease, phosphatase, and catalase activities, which increased by 26.72%, 26.97%, 12.98%, and 54.87%, respectively. NC had a greater effect on soil sucrase, urease, and catalase activities. AC had a strong effect on improving the activity of soil catalase but had little effect on the activities of other enzymes. Under severe Cr stress, BC, AC, and NC significantly improved the activities of soil invertase, urease, and catalase, but only BC increased the activity of soil phosphatase. A comprehensive comparison showed that BC had the greatest effect on improving soil enzyme activity.

3.4. Effects of Different Carbon Types on the Speciation of Cr in Soil

BC, AC, and NC affected the speciation of Cr in the soil, and the results are shown in Table 2. Under natural conditions, the Cr in the soil mainly exists in the speciation of residue, accounting for 57.68% of the total Cr content in the soil, followed by Pre-Cr, accounting for 23.37% of the total Cr content. With the increase in Cr addition, the content of various speciations of Cr in the soil increased, especially the content of Pre-Cr and Res-Cr, which increased significantly. Under different Cr treatment conditions, the application of BC, AC, and NC had little effect on the content of Res-Cr, Pre-Cr, and FeMnO-Cr in the soil, but the content of EXE-Cr and CARB-Cr in the soil decreased, and the Org-Cr content in the soil increased significantly. After BC treatment under different Cr treatment conditions, compared with the control treatment, the content of Org-Cr in the soil increased by 44.09%, 50.13%, and 86.05%, respectively; the content of EXE-Cr decreased by 76.18%, 83.00%, and 75.30%, respectively. The results show that BC, AC, and NC can adsorb Cr in soil, increase the soil organic matter content, increase the proportion of Org-Cr in soil, and reduce Cr bioavailability.

3.5. Effects of Different Carbon Treatments on the Growth and Chlorophyll Fluorescence of Peach Trees under Cr Stress

The increase in Cr content in the soil can significantly reduce the growth and photosynthesis of peach trees. The application of BC, AC, and NC alleviated the toxic effect of Cr on the plants. As shown in Table 3, as the Cr concentration in the soil increased, the chlorophyll content of the plant, the net photosynthetic rate, and the growth of the branches were inhibited. Without exogenous Cr stress, BC, AC, and NC had little effect on plant growth. Under Cr stress conditions, the application of BC, AC, and NC alleviated the adverse effects of Cr on plant chlorophyll content and net photosynthetic rate and promoted shoot growth. The measurement data at different times showed that BC and AC had stronger promoting effects on plant chlorophyll content and photosynthesis under Cr stress conditions; BC had the best effect on promoting plant growth. To further understand the effects of these three carbons on plant photosynthesis, we measured the fluorescence parameters of plant leaves, and the results showed that BC, AC, and NC could increase ΦPSII, Fv/Fm, qP, and Fv/Fo in leaves under Cr stress (Figure S1). BC and AC significantly promoted ΦPSII under severe Cr stress, which increased by 30.95% and 18.53%, respectively, compared with the control (Figure S1A). At the same Cr concentration, the three carbon treatments effectively increased the Fv/Fm value of peach leaves under Cr stress, which was 1.21–1.53 times that of the control (Figure S1B). BC had the most significant effect on improving the qP and Fv/Fo of leaves; compared with the control, it increased by 26.99% and 17.14% under moderate Cr stress, and it increased by 24.34% and 10.03% under severe Cr stress (Figure S1C,D). These results suggest that BC, AC, and NC can alleviate the irreversible or reversible damage of Cr to the PSII reaction center in peach leaves and promote plant growth.

3.6. Effects of Different Carbon Treatments on the Antioxidant Activity of Peach Leaves under Cr Stress

Exogenous Cr stress can cause oxidative damage to peach leaves. As shown in Figure 2D, the MDA content in leaves increased with increasing Cr concentration in the soil. BC, AC, and NC reduced the increase in the MDA content caused by Cr stress, and BC had the best effect. Without exogenous Cr stress, BC, AC, and NC had little effect on the activities of CAT, POD, and SOD in peach leaves (Figure 2A–C). With the increase in soil Cr concentration, the activities of CAT, POD, and SOD in peach leaves first increased and then decreased, indicating that mild Cr stress can activate the protective enzyme system of peach trees and improve the activity of protective enzymes, but high concentrations of Cr inhibited the enzymatic activity. Under Cr stress conditions, NC-treated peach leaves had the highest CAT activity (Figure 2A), and BC-treated leaves had the highest POD and SOD activities (Figure 2B,C). These results indicated that exogenous carbon treatment reduced the degree of peroxidation of the cell membrane and alleviated oxidative stress damage in peach leaves.

3.7. Effects of Different Carbon Treatments on the Concentration of Cr in Peach Trees under Cr Stress

The addition of exogenous Cr had an effect on the growth of peach trees and the accumulation of Cr in various parts. As shown in Figure 3, with the increase in soil Cr concentration, the growth of peach trees was severely inhibited, the dry weight of the shoots and roots decreased (Figure 3A,B), and the Cr accumulation in plants increased (Figure 3C). The BC, AC, and NC treatments alleviated the slow growth of plants and the massive accumulation of Cr in plants caused by Cr stress, and the BC treatment had the best effect. The analysis of Cr content in different parts of the peach tree shows that the Cr content of each part of the plant could increase with the increase in Cr concentration in the soil (Table 4). Under no exogenous Cr stress, BC-, AC-, and NC-treated plants had higher Cr contents in leaves than the control plants and lower Cr contents in the shoots, trunks, and roots. Under Cr stress, the Cr content in all parts of the BC-, AC-, and NC-treated plants was lower than that in the control plants, and the Cr content in the new branch xylem, trunk phloem, and coarse roots decreased most significantly. Comparing the BC, AC, and NC treatments, it was found that BC had the best effect on promoting plant growth and reducing Cr accumulation in plants. In the later stage of the experimental treatment, only the leaves of peach trees in the BC treatment did not fall off, and the content of Cr in each part of the peach trees in the BC treatment was the lowest (Table 4).

4. Discussion

With the development of industry, mining, and agriculture, improper treatment of waste residue and wastewater, and increasing human activities, Cr pollution in farmland soil is becoming increasingly serious. The heavy metal Cr of farmland soil in various administrative regions of China exceeds 36.67% of the local background value [48,49]. One study found that global chrome ore production has been increasing in recent years, increasing the risk of soil chrome pollution. We sampled and analyzed soil from 112 orchards in six major peach-producing areas in China and found that the average soil Cr content was 49.25 mg/kg, and no Cr pollution occurred. However, the soil Cr content in individual production areas is on the rise, and soil Cr pollution is a problem that cannot be ignored [50,51,52].
Carbon is an excellent modifier for the remediation of soil physicochemical properties. It was found that with increasing Cr concentration in the soil, the pH of the soil increased, and the contents of Olsen-P and available N decreased. Additionally, Cr reduced the activities of urease, sucrase, phosphatase, and catalase in the soil. Soil enzymes are important constituents of soil and participate in processes such as soil material transformation, energy metabolism, and pollutant purification [53]. The application of three kinds of carbons can alleviate the adverse effect of Cr on soil. This result is consistent with previous studies on pakchoi and rice [54,55]. Cr disrupts the nutrient balance of the soil and destroys the active structure of soil enzymes, resulting in a decrease in soil enzyme activity. On the one hand, BC, AC, and NC can alleviate Cr pollution because they contain a large amount of carbon, which increases the soil organic matter content, enhances the soil buffer capacity, and regulates pH changes [56]. Soil pH is the most critical factor affecting the availability of soil Cr, and the availability of Cr in soils with pH < 7 is significantly lower than that in soils with pH > 7 [57]. Acidic soil is conducive to the reduction of Cr(VI), which is highly mobile, to Cr(III), which is less mobile, while Cr(III) is more easily oxidized in alkaline soil [20,58,59,60]. On the other hand, these carbon materials have high porosity and a large specific surface area, have good adsorption properties, can reduce the availability of Cr in soil, and can also provide attachment carriers for micro-organisms, providing carbon and nutrient sources for their growth [61,62]. BC, AC, and NC mitigated the decline in soil nutrient availability due to Cr accumulation. After they are added to the soil, these materials have a certain degree of influence on the source, content, form, transformation process, and effectiveness of various elements required for the survival of soil organisms.
The reduction in soil cadmium stress mainly occurs through reducing the soil Cr content and changing the form of Cr ions in two ways [63]. This study found that BC, AC, and NC can all alleviate the adverse effects of Cr accumulation on the growth of peach trees, and the analysis of Cr content and form in soil found that the application of three kinds of carbons reduced the availability of Cr. The carbon materials increased the Org-Cr, FeMnO-Cr, and Pre-Cr contents in the soil and decreased the EXE-Cr and Car-Cr contents but had little effect on the Res-Cr content. Desorption and X-ray photoelectron spectroscopy studies showed that most of the Cr bound to biochar was Cr(III) and that Cr(VI) could be oxidized by light energy groups on the carbon surface. Org-Cr increased and EXE-Cr decreased, indicating that the Cr(VI) content in the soil decreased significantly and the Cr toxicity was weakened [64,65,66]. Among these materials, the effect of BC was the best. This result is consistent with previous research results in rape, pakchoi, and other crops, showing that BC, AC, and NC reduce Cr toxicity by reducing the availability of Cr [54,67]. The analysis found that these three kinds of carbons have a strong adsorption capacity; they have a complete pore structure and large specific surface area; and they can change the form of Cr through physical adsorption, chemical adsorption, and ion exchange reactions, reducing its effectiveness. Compared with AC and NC, BC contains more hydroxyl, carboxyl, carbonyl, and other active functional groups, which can fix heavy metals through surface complexation, thereby forming insoluble and stable metal complexes [68,69,70]. Soil Cr pollution mainly comes from hexavalent Cr(VI), which has high activity in soil and is not easily adsorbed by organic matter and colloids in soil [71]. The modification of Cr speciation by BC, AC, and NC is an important way to reduce Cr toxicity.
Plant biomass is the most direct indicator of plant health. Cr toxicity in plants manifests as yellowing of leaves, curled edges, dwarf plants, slow growth, and even leaf fall-off. With the increase in cadmium concentration in the soil, the symptoms are more obvious [72]. BC, AC, and NC can alleviate the inhibitory effect of Cr poisoning on peach tree growth. Under Cr stress, BC, AC, and NC increased the chlorophyll content, enhanced photosynthesis, and promoted plant growth compared with the control, and this effect was also observed in wheat, rice, and corn [73,74,75]. Chlorophyll fluorescence properties are important indicators of the physiological status of plants under stress conditions. In this experiment, Cr stress caused a decrease in ΦPSII, Fv/Fm, qP, and Fv/Fo of peach saplings, suggesting that Cr damages the photosynthetic system of peach trees, hinders the process of PSII electron transfer, and then leads to the occurrence of photoinhibition. BC, AC, and NC protected the photosynthetic system of leaves, reduced the accumulation of superoxide, and alleviated the peroxidation of the cell membrane and the damage to the cell structure caused by cadmium stress [76]. Behera also found that BC reduced the oxidative stress of Cr in rice and increased the activity of protective enzymes [74]. At the same time, these three carbons promote the growth of peach tree, increase the dry matter mass of the plant, and reduce the Cr content in various parts of the plant. The Cr content in the plant is the most direct criterion for evaluating the effect of the improver. Experiments on a variety of crops have shown that under Cr stress conditions, the lower the accumulation of Cr in plants, the less damage they suffer. This evidence indicates that BC, AC, and NC play important roles in mitigating Cr toxicity in peach trees, with BC being the best.
BC, AC, and NC are all based on carbon and have a large specific surface area, which can adsorb heavy metal ions, and are widely used in pollution control [77]. AC is a kind of microcrystalline carbon material composed of carbon-containing substances with stable chemical properties and great adsorption capacity; NC is a carbon-based nanoscale material with excellent characteristics [37]. BC is prepared by low-temperature pyrolysis and contains large amounts of organic carbon sources [78], which are more beneficial for use in soils. BC has played an important role in alleviating heavy metal stress in crops such as wheat, rice, rape, and berseem clover [79,80,81,82]. This experiment also found that BC had the best effect on alleviating cadmium stress in peach trees. BC can increase the soil organic carbon content, increase the soil nutrient content, and enhance the soil buffer capacity. At the same time, BC can change the form of Cr in soil, reduce the availability of Cr, and reduce the accumulation of Cr in peach trees, thereby reducing the toxic effect of Cr.

5. Conclusions

Soil Cr pollution seriously affects the growth and development of plants, and BC, AC, and NC can effectively alleviate Cr poisoning. This study found that under Cr stress conditions, BC, AC, and NC could increase soil organic matter content, increase soil enzyme activity, change soil Cr speciation, increase Org-Cr, decrease EXE-Cr, and significantly reduce Cr availability. At the same time, they could reduce the accumulation of Cr in peach trees, reduce oxidative stress damage, alleviate the decline in photosynthesis caused by Cr stress, increase the accumulation of dry matter in peach trees, and promote the growth of peach trees, with BC exhibiting the best performance.

Supplementary Materials

In this section, please add: The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/agronomy12112814/s1, Table S1: Chromium content in orchard soils in different regions of China; Figure S1: The effect of BC, AC and NC on chlorophyll fluorescence of peach leaves under Cr stress.

Author Contributions

H.G.: Data curation, Writing—original draft; X.Y.: Conceptualization, Data curation; N.W.: Investigation, Methodology; M.S.: Conceptualization, Investigation; Y.X.: Conceptualization, Methodology, Supervision, Writing—review and editing; F.P.: Conceptualization, Methodology, Project administration, Supervision, Writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the National Key Research and Development Program of China (2020YFD1000203) and the earmarked fund for China Agriculture Research System (No. CARS-30-2-02).

Data Availability Statement

All data supporting the findings of this study are included in the article.

Conflicts of Interest

The authors declare no conflict of interest.

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Agronomy 12 02814 g001 550
Figure 1. The effect of BC, AC, and NC application on soil enzyme activity under Cr stress. (A). The activity of soil sucrase. (B). The activity of soil urease. (C). The activity of soil phosphatase. (D). The activity of soil catalase. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
Figure 1. The effect of BC, AC, and NC application on soil enzyme activity under Cr stress. (A). The activity of soil sucrase. (B). The activity of soil urease. (C). The activity of soil phosphatase. (D). The activity of soil catalase. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
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Figure 2. The effect of BC, AC, and NC application on the antioxidant activity of peach leaves under Cr stress. (A). The activity of catalase. (B). The activity of peroxidase. (C). The activity of superoxide dismutase. (D). The content of malondialdehyde. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
Figure 2. The effect of BC, AC, and NC application on the antioxidant activity of peach leaves under Cr stress. (A). The activity of catalase. (B). The activity of peroxidase. (C). The activity of superoxide dismutase. (D). The content of malondialdehyde. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
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Figure 3. The effect of BC, AC, and NC application on the dry weight and total Cr content of peach trees under Cr stress. (A). The dry weight of shoots. (B). The dry weight of roots. (C). Cr accumulation in peach trees. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
Figure 3. The effect of BC, AC, and NC application on the dry weight and total Cr content of peach trees under Cr stress. (A). The dry weight of shoots. (B). The dry weight of roots. (C). Cr accumulation in peach trees. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
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Table
Table 1. Effects of BC, AC, and NC application on the physicochemical properties of soil under Cr stress.
Table 1. Effects of BC, AC, and NC application on the physicochemical properties of soil under Cr stress.
TreatmentpHOrganic Matter
(g/kg)		Olsen-P
(mg/kg)		Available K
(mg/kg)		Available N
(mg/kg)
Cr0CK6.68 b14.85 ± 0.11 d59.75 ± 2.37 a109.15 ± 4.05 b64.28 ± 2.96 a
Cr0BC6.90 a16.86 ± 0.09 a61.39 ± 1.95 a119.01 ± 5.36 a60.24 ± 2.11 a
Cr0AC6.59 b16.21 ± 0.06 b58.60 ± 2.34 a101.91 ± 3.58 b61.94 ± 2.42 a
Cr0NC6.98 a15.98 ± 0.14 c58.03 ± 2.06 a100.91 ± 5.09 b59.68 ± 2.18 a
Cr100CK6.89 b14.96 ± 0.09 c47.93 ± 1.40 d109.98 ± 4.44 b57.31 ± 2.73 b
Cr100BC6.89 b16.29 ± 0.07 a66.58 ± 1.09 a122.63 ± 5.75 a62.78 ± 2.17 a
Cr100AC6.81 b15.64 ± 0.10 b60.43 ± 2.44 b118.14 ± 3.04 ab61.88 ± 1.59 a
Cr100NC7.15 a15.62 ± 0.11 b56.39 ± 2.01 c119.73 ± 5.72 a63.32 ± 1.11 a
Cr150CK7.36 a14.94 ± 0.08 c42.05 ± 2.10 c110.42 ± 3.20 b54.77 ± 1.35 c
Cr150BC6.99 b16.75 ± 0.08 a60.26 ± 2.99 a125.54 ± 5.09 a61.71 ± 1.65 a
Cr150AC7.03 b15.84 ± 0.08 b55.75 ± 1.42 b121.46 ± 2.69 a58.81 ± 1.10 b
Cr150NC7.08 b15.74 ± 0.09 b54.42 ± 1.95 b122.37 ± 3.82 a58.13 ± 1.60 b
Cr0: Control group, exogenous Cr application at 0 mg/kg; Cr100: Moderate Cr stress, exogenous Cr application at 100 mg/kg; Cr150: Severe Cr stress, exogenous Cr application at 150 mg/kg. BC: BC treatment (0.8% of soil mass); AC: AC treatment (0.8% of soil mass); NC: Nano carbon treatment (3 mL). Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
Table
Table 2. Effect of BC, AC, and NC application on the speciation of Cr in soil.
Table 2. Effect of BC, AC, and NC application on the speciation of Cr in soil.
TreatmentEXE
(mg/kg)		CARB
(mg/kg)		FeMnO
(mg/kg)		Pre
(mg/kg)		Org
(mg/kg)		Res
(mg/kg)
Cr0CK0.382 a1.634 a0.554 c8.758 c4.534 d21.620 a
Cr0BC0.099 c0.396 b0.794 ab9.595 a6.533 a20.245 b
Cr0AC0.094 b0.384 b0.804 a9.515 a6.289 b20.516 b
Cr0NC0.091 b0.388 b0.783 b9.313 b5.993 c20.750 b
Cr100CK1.629 a6.685 a1.542 b53.771 c5.153 d30.614 b
Cr100BC0.256 c3.113 bc2.101 a57.020 a7.736 a31.627 a
Cr100AC0.271 b3.048 c2.164 a55.834 ab7.449 b31.350 a
Cr100NC0.277 b3.261 b2.105 a55.519 b7.162 c30.708 b
Cr150CK3.196 a14.358 a2.759 c70.321 c7.259 d52.152 b
Cr150BC0.789 c7.375 d3.702 a74.313 a13.506 a53.853 a
Cr150AC0.788 c7.670 c3.620 a73.223 ab12.557 b53.005 ab
Cr150NC0.860 b8.041 b3.494 b72.939 b11.979 c52.278 b
EXE: exchange state; CARB: carbonate-binding state; FeMnO: iron–manganese-oxide-binding state; Pre: precipitation state; Org: organic-binding state; Res: residue state. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
Table
Table 3. Effects of BC, AC, and NC application on the growth of peach trees under Cr stress.
Table 3. Effects of BC, AC, and NC application on the growth of peach trees under Cr stress.
TreatmentsChlorophyll Content
(mg/g)		Static Photosynthetic Rate (nmmol/m2/s)Growth of Girth of Trunk (mm)Shoot Growth
(cm)
6.157.158.156.157.158.156.1–8.16.1–8.1
Cr0CK2.77 a3.25 a2.07 c10.37 a11.69 b8.77 b3.14 a9.33 d
Cr0BC2.78 a3.27 a2.22 a10.74 a12.02 a9.06 a3.20 a11.85 a
Cr0AC2.75 a3.21 ab2.16 b10.57 a11.75 ab8.80 b3.11 a10.53 c
Cr0NC2.78 a3.17 b2.16 b10.66 a11.52 b8.76 b3.14 a11.05 b
Cr100CK2.22 b2.91 b1.72 b7.33 b8.36 c7.02 b1.88 b4.67 d
Cr100BC2.47 a3.08 a1.81 a8.78 a9.37 a8.35 a2.08 a6.90 a
Cr100AC2.43 a3.09 a1.76 ab8.75 a9.14 b8.23 a2.05 a6.05 b
Cr100NC2.42 a3.08 a1.79 a8.60 a9.11 b8.31 a1.93 b5.75 c
Cr150CK2.15 c2.73 b1.61 b5.77 c7.36 c5.03 c1.72 b2.04 d
Cr150BC2.41 a2.85 a1.69 a7.16 a8.02 a6.25 a1.88 a3.40 a
Cr150AC2.38 ab2.83 a1.70 a6.95 b7.69 b5.96 b1.82 a2.75 b
Cr150NC2.35 b2.80 ab1.71 a6.96 b7.71 b5.99 b1.85 a2.44 c
Chlorophyll content and static photosynthetic rate were measured on 15 June, 15 July, and 15 August; growth of the girth of trunk and shoot growth were measured from 1 June to 1 August. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
Table
Table 4. Effects of BC, AC, and NC application on the concentration of Cr in peach trees under Cr stress.
Table 4. Effects of BC, AC, and NC application on the concentration of Cr in peach trees under Cr stress.
TreatmentLeaf (mg/kg)New Branch Phloem (mg/kg)New Branch Xylem
(mg/kg)		Trunk Phloem (mg/kg)Trunk Xylem (mg/kg)Coarse
Root (mg/kg)		Fine
Root
(mg/kg)
Cr0CK3.038 d6.642 a5.831 a25.371 a8.028 a10.757 a53.812 a
Cr0BC4.645 b4.356 b2.395 d20.692 b6.194 c8.461 c45.606 c
Cr0AC4.895 a4.488 b2.588 c18.724 c4.505 d10.587 a48.887 b
Cr0NC4.029 c3.808 c3.079 b21.001 b6.752 b8.962 b46.362 c
Cr100CK63.037 a44.713 a21.426 a264.354 a94.822 a543.215 a626.183 a
Cr100BC37.789 c26.869 d11.167 d156.280 d65.985 c282.904 d331.069 d
Cr100AC47.883 b34.371 c13.927 c176.192 c75.514 b330.849 c390.916 b
Cr100NC50.924 b37.799 b15.967 b189.551 b76.727 b361.797 b356.545 c
Cr150CK----106.155 a73.792 a875.618 a225.038 a736.881 a951.911 a
Cr150BC86.85684.613 d33.472 c372.397 d181.677 c430.132 c562.478 c
Cr150AC----89.154 c34.549 bc387.716 c179.954 c464.695 b594.519 c
Cr150NC----96.376 b36.530 b484.010 b198.847 b435.219 c658.880 b
On September 15, the whole plant was sampled and analyzed to determine the Cr content of each part. Data represent the means of three replicates ± SEs, and different letters indicate significant differences (p < 0.05).
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Gao, H.; Yang, X.; Wang, N.; Sun, M.; Xiao, Y.; Peng, F. Effects of Different Carbon Types on the Growth and Chromium Accumulation of Peach Trees under Chromium Stress. Agronomy 2022, 12, 2814. https://doi.org/10.3390/agronomy12112814

AMA Style

Gao H, Yang X, Wang N, Sun M, Xiao Y, Peng F. Effects of Different Carbon Types on the Growth and Chromium Accumulation of Peach Trees under Chromium Stress. Agronomy. 2022; 12(11):2814. https://doi.org/10.3390/agronomy12112814

Chicago/Turabian Style

Gao, Huaifeng, Xiaoqing Yang, Nana Wang, Maoxiang Sun, Yuansong Xiao, and Futian Peng. 2022. "Effects of Different Carbon Types on the Growth and Chromium Accumulation of Peach Trees under Chromium Stress" Agronomy 12, no. 11: 2814. https://doi.org/10.3390/agronomy12112814

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