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Article

Cunninghamia lanceolata (Lambert) Hooker: A Promising Candidate for Phytoremediation of Cd-Contaminated Soils

by
Dachuan Dai
1,
Hongling Hu
1,*,
Jing Wen
1,
Hong Chen
2,
Gang Chen
1 and
Xinglei Cui
1
1
College of Forestry, Sichuan Agricultural University, Chengdu 611130, China
2
College of Agricultural Sciences, Xichang University, Xichang 615000, China
*
Author to whom correspondence should be addressed.
Forests 2024, 15(1), 115; https://doi.org/10.3390/f15010115
Submission received: 12 November 2023 / Revised: 12 December 2023 / Accepted: 21 December 2023 / Published: 7 January 2024
(This article belongs to the Section Forest Soil)
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Abstract

:
Cadmium (Cd) is one of the most common toxic heavy metal elements in soil pollution, which can be continuously enriched in the food chain and eventually threaten human health. Phytoremediation, which is using plants to transfer heavy metal elements from soils, is a promising solution for the remediation of heavy metal-contaminated soils. In this study, we evaluated whether Cunninghamia lanceolata (Lambert) Hooker (Chinese fir), a widely planted timber tree worldwide, had the potential to remediate Cd-contaminated soils through 90 days pot of experiments with different Cd concentration soils (0, 5, 10, 20, 50, 100 mg kg−1). C. lanceolata did not show obvious toxic symptoms in Cd-contaminated soils, although Cd inhibited plant growth and decreased net photosynthetic rate slightly. The activities of antioxidant enzymes increased significantly under Cd stress, indicating that C. lanceolata had a strong self-regulation ability and can tolerate Cd stress. The Cd bioconcentration factor (Cd concentration in plant divided by Cd concentration in soil) of C. lanceolata were greater than 1 at all Cd concentrations, indicating that C. lanceolata had a strong ability to absorb Cd, although Cd was mainly accumulated in roots. Our results indicated that C. lanceolata had a strong tolerance and phytostabilization ability of Cd. Considering the wide distribution worldwide, large biomass, and rapid growth of C. lanceolata, it could be a promising candidate for phytoremediation of Cd-contaminated soils.

1. Introduction

With the process of industrialization and urbanization, the problem of heavy metal contamination in soils is becoming more and more serious [1,2]. Cadmium (Cd), which has high toxicity, large solubility in water, high mobility in the soil replacement system, and can be continuously enriched in the food chain, is one of the most hazardous heavy metals in the environment [3,4]. Once consumed by human beings, Cd will lead to chronic toxicity and pose a serious threat to human health, such as disrupting calcium metabolism, leading to hypercalciuria and the formation of kidney stones [5,6,7]. Cadmium pollution has become a worldwide problem that affects resources for food and drinking water mainly in Asia and Africa.
Phytoremediation is the use of plants to extract, sequester, and/or detoxify heavy metal elements and is a promising solution for the remediation of heavy metal contaminated soils due to its low cost, environmental friendliness, ease of operation, and wide applicability [8,9]. Phytoremediation can be divided into two main types, phytoextraction and phytostabilization. Phytoextraction refers to the uptake of soil heavy metals through the below-ground of the plant and accumulation in the above-ground, which is then collected and disposed of as hazardous waste or incinerated to recover the metals [10]. While phytostabilization reduces the mobility and bioavailability of heavy metals in the soil by immobilizing the metals at the plant rhizosphere through chelation (binding and adsorption) processes. The purpose of phytostabilization is to stabilize heavy metals and reduce the risk to human health and the environment, rather than remove heavy metals from polluted soil [11].
Plants used in phytoextraction that can accumulate high concentrations of heavy metals in the aboveground parts are called hyperaccumulators [12]. So far, hundreds of heavy metal hyperaccumulators have been identified, but most of them are herbaceous plants [13,14]. Although herbaceous plant species can accumulate high concentration of heavy metals, the total amount of heavy metals they can accumulate is limited due to their low biomass [15]. Furthermore, their low economic value and ease of entry into the food chain by livestock and poultry limited their application [16,17]. Fast-growing woody plants, which have the advantages of rapid growth, large biomass, well-developed roots, high tolerance to heavy metal stress, extensive uptake of different heavy metals, and do not enter the food chain of human beings [18,19], have the potential for phytostabilization of contaminated soil. In recent years, fast-growing woody plants such as Populus deltoides W.Bartram ex Marshall [20] and Salix viminalis L. [21] have been reported to be used for phytostabilization of heavy metal contaminated soil, but compared with herbaceous hyperaccumulators, there are few woody plants have been identified and applied for phytostabilization, indicating an area with significant potential for further research and application.
Cunninghamia lanceolata (Lambert) Hooker (Chinese fir), which is an evergreen sub-tropical conifer species with high timber yield, excellent timber quality, and rapid growth, accounted for 6.1% of the total global plantation area by 2015 [22]. In China, Chinese fir is the most widely planted species, with an area of 9.87 million hectares, accounting for 1/4 of the total plantation area in China [23,24]. Previous studies have found that Chinese fir could grow in heavy metal contaminated sites and have a good ability to develop and adapt under these conditions [25,26]. Given the wide distribution, substantial biomass, and rapid growth exhibited by C. lanceolata, these properties have attracted considerable interest in the remediation of contaminated soils. However, the tolerance and accumulation of Cd in C. lanceolata have been scarcely publicly reported. The aims of this study are: (1) estimate the Cd tolerance of C. lanceolata; (2) measure the accumulation ability of Cd in different C. lanceolata organs; (3) evaluate the feasibility of C. lanceolata for the remediation of Cd contaminated soils. The results will provide some theoretical basis and data reference for the further application of phytoremediation in cadmium-contaminated areas.

2. Materials and Methods

2.1. Plant Management and Growth Conditions

The experiment was conducted at the teaching and research station of Sichuan Agricultural University. Its geographical coordinates are 103°51′29″ E and 30°42′18″ N.
C. lanceolata seedlings were collected from the State-owned Forest Farm in Hongya County, Sichuan Province of China. Healthy seedlings with similar size at 1 year were selected and transplanted into the pots filled with nutrient-rich soil (1 seedling per pot) for 60 days of acclimatization. Seedlings were irrigated every 2–3 days and soil moisture was monitored using a HH2 soil moisture meter (ML2x, GBR) to maintain field water holding capacity at 80% of the saturated soil water capacity. Add 4 g of NPK compound fertilizers (15% N, 15% P2O5, 15% K2O) to each pot every 20 days to promote seedling growth.
The planting substrate was yellow soil collected from the same forest farm. Its chemical properties (5 replicates) were pH 5.75 ± 0.32, total nitrogen 4.62 ± 0.24 g kg−1, total potassium 15.63 ± 0.75 g kg−1, total phosphorus 1.45 ± 0.17 g kg−1, cadmium 0.36 ± 0.04 mg kg−1. The planting container was a polyethylene plastic pot with four drainage holes drilled in the bottom, 25 cm diameter at the top, 20 cm diameter at the bottom, 23 cm high, and the dry weight of the substrate in each pot was 10 kg.

2.2. Experimental Design

0, 10, 20, 50, and 100 mg Cd kg−1 (supplied as CdCl2 2.5H2O aqueous solution, the mass was calculated based on the molecular weights and the dry weight of the soil, then add enough water to dissolve it completely) were added to the soils, respectively. After the addition of cadmium solution, the substrate was thoroughly mixed to ensure homogeneity and kept in equilibrium for 30 days. After 60 days of acclimatization, seedlings were transplanted into the soil with a Cd concentration gradient. Five replicates were established for each treatment, and all treated plants were placed in a greenhouse. Water management as above, stop fertilizer application. Place a plastic tray at the bottom of the pot to collect any cadmium solution that may have leaked and pour it back into the soil. Once every half a month, the positions of each treatment in the greenhouse were randomly exchanged.
Height and ground diameter of all seedlings were measured before Cd treatment, and index measurement was carried out 90 d after Cd application. LI-6800 portable photosynthesis system (LI-COR Inc., Lincoln, NE, USA) was used to measure gas exchange parameters. Leaves from seedlings were picked, sealed, and labeled, then placed in ice boxes and brought back to the laboratory for determination of chlorophyll content, physiological, and biochemical properties. Thereafter, seedling height and diameter were measured, followed by the harvest of seedlings for determination of cadmium content in organs of leaves, stems, and roots.

2.3. Determination of Plant Physiological and Biochemical Indices

2.3.1. Growth Traits

Seedling height (0.01 cm) was determined using a tape, and basal diameter (0.01 mm) was determined with a vernier caliper. Leaves, stems, and roots of seedlings were harvested, washed, and then dried at 80 °C to constant weight. Dry weights were measured for each organ.

2.3.2. Photosynthetic Parameters

Photosynthetic pigments content: the sampled leaves were wiped clean, cut, and immersed in an extract of 80% (v/v) acetone to extract photosynthetic pigments, and the mixture was placed in the dark and left for more than 24 h until the leaves were completely white [27]. Light absorbance was measured at 663, 645, and 470 nm using a spectrophotometer (UV-4802H, UNICO Inc. Shanghai, China), and the chlorophyll a (Chl a), chlorophyll b (Chl b), and carotenoid (car) contents were calculated as described by [28]:
Ca = 12.71 × A663 − 2.59 × A645
Cb = 22.88 × A645 − 4.67 × A663
Cc = (1000 × A470 − 3.27 × Ca − 104 × Cb)/229
where Ca, Cb, and Cc represent the contents of chlorophyll a, chlorophyll b, and carotenoid, respectively, and A663, A645, and A470 represent the absorbances of the corresponding wavelength.
Gas exchange parameters: the gas exchange parameters were measured using a LI-6800 portable photosynthesis system. The CO2 concentration was set at 400 μmol mol−1, the leaf chamber temperature at 30 °C, the relative humidity at 60%, and the photosynthetic active radiation (PAR) at 800 μmol m−2 s−1. The net photosynthetic rate (Pn), transpiration rate (Tr), stomatal conductance (Gs), and intercellular CO2 concentration (Ci) of the middle part of the second fully expanded leaves were measured between 9:00 and 11:30 AM. Three plants were randomly selected for each treatment, and three leaves were determined for each plant.
Chlorophyll fluorescence: the same LI-6800 portable photosynthesis system was adopted for measurement, and the settings and leaf sampling were the same as above. The sampled leaves were dark adapted for 1 h and then the minimal fluorescence level (F0) and maximum fluorescence level (Fm) were measured. Afterward, the actinic light was turned on and photo-activated until the fluorescence parameter was stable, and then the steady-state fluorescence (Fs), minimum fluorescence level in a light-adapted state (F0’), and maximum fluorescence level in a light-adapted state (Fm’) were measured. The following parameters were also measured or calculated simultaneously, Fv/F0: the ratio of photochemical to non-photochemical processes in PSII, Fv/Fm: the maximum photochemical efficiency of PSⅡ, Fv’/Fm’: the effective quantum yield, ΦPSⅡ: the actual quantum yield, ETR: the electron transfer rate, qP: the photochemical quenching coefficient, and NPQ: the non-photochemical quenching coefficient [29,30].

2.3.3. Determination of Antioxidant Parameters

0.3 g of fresh leaves were washed, cut, and ground in a mortar thoroughly with liquid nitrogen. The ground leaves were then homogenized with 10 mL phosphate buffer, followed by centrifugation at 10,000 r/min for 15 min at 4 °C, the supernatant was collected as the test sample. SOD was tested by evaluating the inhibition of nitro blue tetrazolium reduction [31]. One unit of SOD activity was considered as the amount of SOD activity that inhibits 50% of nitro blue tetrazolium in the photoreduction reaction (at 560 nm). CAT was assessed by measuring the reduction in H2O2 [32], and one unit of CAT activity was defined as a reduction of 0.1 units per minute at 240 nm. POD was assayed by the oxidation of guaiacol under H2O2 (at 470 nm) [33]. All antioxidant enzymatic activities were presented as U g−1 fresh weight (FW). The H2O2 content was determined using a method based on the formation of colored [TiO(H2O2)]2+ complexes (specific absorption peak of 410 nm) by H2O2 and titanium ions [34]. Free proline (Pro) was extracted with sulfosalicylic acid and determined by acidic ninhydrin colorimetric assay [35]. Determination of malondialdehyde (MDA) and soluble sugar content (SS) by heated colorimetric method using thiobarbituric acid [36]. The content or activities of all the above parameters were measured according to kit instructions (Jiancheng Bioengineering, Nanjing, China).

2.3.4. Concentration of Cd

The dried plant and soil samples (0.3 g) were crushed, ground, and passed through 1 mm sieve. These samples were then digested with 10 mL mixture of HNO3/HClO4 (4:1, v/v) at 170 °C [37], and the volume was brought to 50 mL with deionized water. The Cd contents in plant and soil were determined using a NexION 1000G ICP-mass spectrometer (Perkin Elmer Inc. Waltham, MA, USA). For quality assurance/control, the measured Cd values were verified using the GBW07603 (GSV-2; plants twigs and leaves) and GBW07428 (GSS-14; Sichuan basin soil) from the Center of National Standard Reference Materials of China (CNSRMC).

2.3.5. Calculation Formula

The root/shoot ratio was calculated according to the equations [38]: root/shoot ratio = Broot/Bshoot, where Broot and Bshoot was the root biomass and shoot biomass. The phytoextraction ability was determined using the translocation factor (TF) and the bioconcentration factor (BCF) according to the equations [39]: TF = Cshoot/Croot, BCF = Cshoot/Csoil or Croot/Csoil, where Cshoot, Croot, and Csoil was Cd concentration (mg kg−1) in the shoot, root, and soil, respectively.

2.4. Statistical Analysis

Significant differences between groups were determined by one-way analysis of variance (ANOVA) with Duncan’s test, which was carried out using SPSS 27 (IBM Inc., Chicago, IL, USA), and means and standard errors were also calculated using SPSS 27. Using Origin 2022 (Origin Lab Inc., Northampton, MA, USA) for correlation analysis and graph drawing.

3. Results

3.1. The Growth and Cd Tolerance of C. lanceolata

In this study, we found that the total biomass and Pn (net photosynthetic rate) of C. lanceolata decreased with the increase of Cd concentration in soil, while the activities of antioxidant enzymes SOD (superoxide dismutase), POD (peroxidase), and CAT (catalase) increased (Figure 1).
Specifically, the addition of Cd significantly inhibited the height, basal diameter, and biomass of C. lanceolata (p < 0.05), while the effect was slight when Cd concentration was low (Table 1). For example, plant height was not significantly affected when the concentration of Cd was less than 10 mg kg−1. Cd had no significant effect on the growth of basal diameter when the concentration of Cd was less than 50 mg kg−1. Both root and shoot biomass were reduced by Cd stress, but the biomass of any given organs was not significantly influenced when the Cd concentration was less than 20 mg kg−1, which indicated that low concentrations of Cd had a slight effect on the growth of C. lanceolata.
Chlorophyll content (chlorophyll a, chlorophyll b) and Pn decreased significantly with the increase of Cd (Table 2). When the Cd concentration of soil was more than 50 mg kg−1, the contents of chlorophyll a, chlorophyll b, and total chlorophyll were significantly reduced. Gs, Tr, and ΦPSII also decreased significantly with the increase of Cd, while Ci, Fv/Fm, and Fv’/Fm’ did not change significantly (Table 2).
H2O2 increased significantly with the increase of soil Cd concentration (p < 0.05), and H2O2 content was 2.18 times higher than that of the control when soil Cd concentration was 100 mg kg−1 (Table 3). As a product of lipid peroxidation, the content of MDA increased slightly with the aggravation of Cd stress, however, there was no significant effect on the content of MDA when the soil Cd content was lower than 50 mg kg−1. Similarly, to the antioxidant enzymes (SOD, POD, and CAT), the contents of proline and soluble sugar were also increased with the increase of Cd concentrations (Table 3).

3.2. Cd Uptake and Accumulation Characteristics of C. lanceolata

The Cd contents in stems, leaves, roots, and shoots of C. lanceolata seedlings increased significantly with the increase of soil Cd content, particularly when exceeding 20 mg kg−1. The Cd contents in roots were much higher than those in other organs and the bioconcentration factor (BCF) of C. lanceolata roots was 6.01–11.29 (Table 4, Figure 2). Under different soil Cd concentrations, the bioconcentration factor (BCF) of C. lanceolata plants was lager than 1 (2.47–4.77) and showed slight variation (Figure 2). The Cd accumulation amounts in shoots and roots of C. lanceolata seedlings increased linearly with the increase of Cd concentration in soil (r2 for shoots = 0.9364, r2 for roots = 0.9641; Figure 3). When the soil Cd concentration reached 100 mg kg−1, the total Cd accumulation amount in shoots and roots were 2.72 mg plant−1 and 19.34 mg plant−1, respectively (Figure 3). This study also found that the translocation factor (TF) of C. lanceolata did not vary significantly with the increase of Cd in soils (Table 4).

4. Discussion

Phytoremediation, the use of plants for environmental cleanup, has been accepted as a cost-effective and environmentally friendly remediation strategy [40]. Cd is highly toxic to plants and animals and is one of the most common metal elements that has contaminated large areas of soils [4]. When the concentration of Cd in the soil exceeds 8 mg kg−1, growth retardation and other toxic symptoms are easily observed in most plant species [41]. When the concentration of Cd in soil reached 25 mg kg−1, the growth of most Cd accumulators and hyperaccumulators decreased significantly [34,42], due to Cd destroying plant roots, reducing the absorption of water and nutrients [43,44]. In this study, we found that although the growth of C. lanceolata seedlings decreased under Cd stress, the seedlings did not show obvious toxic symptoms during the experimental period (Supplementary Figure S1). In addition, the root and shoot biomass showed some variations at soil Cd concentrations from 0–20 mg kg−1, but not significantly, indicating that low concentrations of soil Cd did not inhibit the growth of C. lanceolata too much.
The growth and development of plants are mainly modulated by photosynthesis in plants [35]. Many studies have shown that Cd would accelerate the degradation of chlorophyll, reduce stomatal opening, decrease electron transfer rate, and finally affect photosynthetic capacity [9,34,45]. Although chlorophyll a, chlorophyll b, and Pn in C. lanceolata leaves gradually decreased with the increase of soil Cd concentrations, the Pn did not decrease significantly (Table 2) when the soil Cd concentrations were lower than 10 mg kg−1. In this study, the Gs, Tr, and Ci of C. lanceolata decreased significantly, and the decrease of Gs, Tr, and Ci were other possible reasons that limited Pn (called stomatal factor limitation) [46]. Similar results were found in Morus alba L. [34], Prosopis juliflora (Swartz) DC. [47], and Sassafras tzumu (Hemsl.) Hemsl. [48]. The values of Fv/Fm in most plant species are usually between 0.75 and 0.85 [49,50], which indicates a high photochemical activity of PSⅡ in C. lanceolata, Fv/Fm decreased slightly under Cd stress, but were all greater than 0.80 and did not differ significantly between treatments. The results revealed that Cd stress had a slight influence on photosynthetic apparatus and supported that the stomatal factor was the main reason for the decrease in Pn. ΦPSⅡ is the proportion of absorbed light energy actually used for photochemistry, and qP indicates the proportion of PSⅡ reaction centers that are open [51]. The results showed that ΦPSⅡ decreased significantly with the increase of Cd concentration, indicating that less and less absorbed light energy was used for photochemistry at the reaction center of PSII.
H2O2 is a potent signaling molecule with multiple roles in plant antioxidant defense, such as causing systemic acquired resistance (SAR) and hypersensitive resistance (HR) to improve their immunity [52]. In this study, the H2O2 content increased gradually with the increase of Cd concentration, indicating that C. lanceolata seedlings improved their resistance to Cd stress by inducing the production of H2O2. MDA is a representative index to measure lipid peroxidation induced by oxidative stress [53]. Cd stress caused a gradual increase of MDA content in C. lanceolata seedlings, but it was significantly higher than the control only when the Cd concentration was 100 mg kg−1, indicating that low concentrations of Cd did not cause oxidative stress on C. lanceolata seedlings.
Heavy metal stress will lead to the increase of ROS content such as superoxide anion (O2−), which will cause oxidative damage to biomolecules like lipids, proteins, and nucleic acids. Antioxidant enzymes, such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), can be improved by excess ROS and facilitate the removal of ROS [54]. Among these enzymes, SOD serves as the first line of defense, which converts O2− into H2O2 and O2; subsequently, H2O2 decomposes into H2O by the action of CAT, the main H2O2 scavenging enzyme [55,56]. POD is considered to be the last line of defense for H2O2 removal [57]. SOD, CAT, and POD activity in C. lanceolata leaves increased gradually with the increase of Cd concentration. Similar results were found in Salix matsudana Koidz. [58], Populus × euramericana (Dode) Guinier [59], and Populus yunnanensis Dode [60]. The content of proline and soluble sugar also increased significantly under Cd stress. Proline and soluble sugar are important compatible solutes in osmoregulation, which enhances plant tolerance to heavy metal stress through different mechanisms such as cellular osmotic adjustment, membrane integrity protection, quenching singlet oxygen atoms, metal chelation in the cytoplasm, and protection of enzymes against denaturation [61,62]. The increases in proline and soluble sugar indicated that Cd stress induced the synthesis of osmolytes in C. lanceolata leaves to maintain osmotic balance and enhanced resistance to stress.
Except tolerance, absorption, and translocation abilities of metal elements are other criteria for determine whether a plant species can be used in phytoremediation. BCF, which describes the ability of plants for heavy elemental accumulation from the substrate, is an important parameter for judging the phytoremediation potential of a given plant [63,64]. In our study, the BCF values of C. lanceolata were around 4, indicating that C. lanceolata has a strong capacity for Cd uptake and accumulation, as previously reported Cd hyperaccumulators usually had a value of BCF from 1.5–5, such as Populus deltoides [20] is 3.0, Youngia japonica (L.) DC. [65] is 5.2, Juncus bufonius L. [38] is 3.9. TF, which assesses the ability of plants to transfer heavy metals from roots to shoots, is another commonly used parameter to evaluate the phytoremediation potential of a given plant [66,67]. In C. lanceolata, the TF values under Cd stress ranged from 0.07–0.11, which implied that C. lanceolata has a weak ability to transfer Cd from roots to shoots. However, lower TF values imply a low shoots Cd content, which can prevent wildlife exposure and surface contamination, which is one of the candidate plant criteria for phytostabilization [68]. Besides, Fan [69] and Taamalli [70] hypothesized that plants restricted the translocation of Cd to the aboveground parts to avoid damage to the aboveground parts and maintain normal plant growth. Yoon et al. [71] found that most plants growing on a contaminated site in North Florida had high BCF values but low TF values, but suggested that these plants still had high potential for phytoremediation and could be considered as potential phytoremediation plants. Considering the high BCF and rapid growth of C. lanceolata, it still has great potential for Cd phytoremediation.
The soil Cd concentrations in most polluted areas generally do not exceed 50 mg kg−1 [72,73]. When the soil Cd concentration was below 50 mg kg−1, C. lanceolata seedlings did not show significant biomass reduction or visible symptoms of toxicity as well as high physiological and biochemical tolerance, allowed C. lanceolata to produce large amounts of biomass and grow rapidly enough to establish vegetative cover in time at a specific location. In the field, the huge canopy of C. lanceolata helps to reduce eolian dispersion, while the dense and deep root system helps to prevent water erosion and leaching, which creates a vegetative cap to achieving long-term stabilization of Cd-contaminated soil [23,68]. These findings indicated that C. lanceolata is a promising candidate for phytostabilization of Cd-contaminated soils, especially in non-severely contaminated soils with Cd concentrations below 50 mg kg−1.
Our findings offer compelling evidence of Cd tolerance and accumulation in C. lanceolata, suggesting its potential as a candidate for remediating Cd contaminated soils. However, it is important to note some limitations in our study. Our study was carried out on pot experiments, this can diminish susceptibility to environmental factors and experimental errors, thereby enabling the acquisition of objectively reliable data that can be replicated and compared. However, pot experiments may not fully replicate the intricate interactions and dynamic factors present in natural flora environments. Consequently, future research endeavors should extend beyond pot experiments to field studies in natural areas. Furthermore, a more in-depth investigation into the physiological and genetic mechanisms underlying the tolerance to and accumulation of Cd in C. lanceolata is warranted.

5. Conclusions

Cunninghamia lanceolata had high tolerance to Cd at physiological (e.g., photosynthesis characteristics and chlorophyll fluorescence parameters) and biochemical levels (e.g., oxidative stress markers and antioxidant enzyme), with strong Cd accumulation (predominance in roots). Considering the wide distribution, fast growth, large biomass, and high economic value, we suggested that C. lanceolata could be a promising candidate for the phytostabilization of Cd contaminated soils.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f15010115/s1.

Author Contributions

This idea was developed by H.H. and D.D. led the writing of the manuscript, with critical input from J.W., H.C., G.C. and X.C. All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by the Breeding Research Project of Sichuan Province during the 13th Five-year Plan period (2016 NZ0098-10), Key Project of Sichuan Education Department (13ZA0246).

Data Availability Statement

Data presented in this study are available from the authors upon request.

Conflicts of Interest

The authors declare no conflict of interest.

Abbreviations

Cd, cadmium; BCF, bioconcentration factor; CAT, catalase; Car, carotenoids; Chl, chlorophyll; Pn, net photosynthetic rate; Gs, stomatal conductance; Tr, transpiration rate; Ci, intercellular CO2 concentration; Fv/Fm, maximal quantum yield of PSII; Fv’/Fm’, photochemical efficiency of PSII; ΦPSII, Actual photochemical efficiency of PSII; H2O2, hydrogen peroxide; MDA, malondialdehyde; ROS, reactive oxygen species; SOD, superoxide dismutase; TF, translocation factor.

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Forests 15 00115 g001
Figure 1. Main tolerance parameters of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations. Error bars show the standard error of the mean values (n = 5).
Figure 1. Main tolerance parameters of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations. Error bars show the standard error of the mean values (n = 5).
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Figure 2. BCF of C. lanceolata seedlings at different soil Cd concentrations. Error bars show the standard error of the mean values (n = 5).
Figure 2. BCF of C. lanceolata seedlings at different soil Cd concentrations. Error bars show the standard error of the mean values (n = 5).
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Forests 15 00115 g003
Figure 3. Cd accumulation amount in shoots and roots of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations. Error bars show the standard error of the mean values (n = 5).
Figure 3. Cd accumulation amount in shoots and roots of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations. Error bars show the standard error of the mean values (n = 5).
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Table 1. Growth of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations.
Table 1. Growth of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations.
Concentration
of Cd
mg kg−1		Net Growth in
Plant Height
cm		Net Growth in
Basal Diameter
mm		Root Biomass
g plant−1		Leaf Biomass
g plant−1		Stem Biomass
g plant−1		Shoot Biomass
g plant−1		Total Biomass
g plant−1
046.46 ± 1.50 a6.36 ± 0.26 a33.59 ± 6.51 a27.73 ± 2.00 a23.41 ± 1.25 a51.13 ± 3.24 a84.73 ± 6.03 a
542.45 ± 5.05 ab6.04 ± 0.56 a25.41 ± 2.16 ab25.19 ± 2.61 ab21.93 ± 2.94 a47.12 ± 4.93 a72.53 ± 4.57 b
1037.54 ± 4.24 abc5.74 ± 0.56 ab23.96 ± 3.71 ab23.47 ± 1.10 ab19.35 ± 1.71 ab42.82 ± 2.68 abc66.79 ± 4.16 bc
2035.10 ± 1.07 bc5.68 ± 0.52 ab25.36 ± 1.44 ab25.03 ± 1.34 ab19.61 ± 1.33 ab44.64 ± 2.08 ab70.00 ± 2.27 b
5030.20 ± 4.15 c5.35 ± 0.51 ab20.43 ± 1.17 b20.23 ± 1.22 b15.28 ± 2.18 b35.50 ± 2.77 bc55.93 ± 2.82 cd
10027.76 ± 1.56 c4.17 ± 0.61 b19.95 ± 1.98 b20.53 ± 0.92 b14.04 ± 0.96 b34.57 ± 1.54 c54.52 ± 2.43 d
Note: Data are presented as the mean values ± standard error (n = 5). Different lowercase letters indicate significant differences between treatments at p < 0.05.
Table 2. Photosynthetic parameters of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations.
Table 2. Photosynthetic parameters of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations.
Concentration of Cd in Soil
mg kg−1		Content of
Chl a
mg g−1		Content of
Chl b
mg g−1		Total Content of Chlorophyll
mg g−1		Pn
μmol m−2 s−1		Tr
mmol m−2 s−1		Ci
μmol mol−1		Gs
mol m−2 s−1		Fv/FmFv’/Fm’ΦPSⅡ
00.986 ± 0.119 a0.254 ± 0.039 a1.239 ± 0.158 a4.38 ± 0.22 a1.29 ± 0.09 a276.24 ± 7.67 a0.07 ± 0.01 a0.801 ± 0.016 a0.494 ± 0.032 a0.111 ± 0.020 a
50.943 ± 0.111 a0.233 ± 0.028 ab1.175 ± 0.139 a3.47 ± 0.27 ab0.89 ± 0.11 b247.89 ± 9.08 a0.04 ± 0.00 b0.795 ± 0.010 a0.465 ± 0.022 a0.104 ± 0.008 a
100.779 ± 0.075 ab0.190 ± 0.021 abc0.969 ± 0.096 ab3.36 ± 0.40 ab0.70 ± 0.05 bc236.21 ± 27.41 a0.03 ± 0.00 bc0.803 ± 0.011 a0.468 ± 0.061 a0.088 ± 0.006 a
200.745 ± 0.050 ab0.178 ± 0.012 bc0.923 ± 0.062 ab2.65 ± 0.19 bc0.57 ± 0.02 c236.66 ± 30.87 a0.02 ± 0.00 c0.788 ± 0.006 a0.460 ± 0.014 a0.051 ± 0.005 b
500.651 ± 0.018 b0.155 ± 0.008 c0.806 ± 0.025 b2.70 ± 0.37 bc0.50 ± 0.05 c233.02 ± 14.52 a0.03 ± 0.00 c0.799 ± 0.006 a0.395 ± 0.009 a0.042 ± 0.002 b
1000.618 ± 0.039 b0.151 ± 0.013 c0.769 ± 0.049 b2.23 ± 0.38 c0.53 ± 0.05 c225.51 ± 17.19 a0.02 ± 0.00 c0.786 ± 0.009 a0.366 ± 0.068 a0.046 ± 0.007 b
Note: Data are presented as the mean values ± standard error (n = 5). Different lowercase letters indicate significant differences between treatments at p < 0.05.
Table 3. The oxidative stress markers and antioxidant enzyme activities of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations.
Table 3. The oxidative stress markers and antioxidant enzyme activities of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations.
Concentration of Cd
mg kg−1		MDA
mmol g−1		H2O2
μmol g−1		POD
U g−1		CAT
U g−1		SOD
U g−1		Pro
μmol mol−1		SS
mmol g−1
00.05 ± 0.00 b180.20 ± 10.54 c330.51 ± 6.63 c69.60 ± 0.31 c1120.47 ± 60.41 d0.85 ± 0.04 d0.31 ± 0.03 c
50.06 ± 0.00 ab238.31 ± 13.05 bc369.54 ± 2.95 b71.69 ± 0.58 c1398.31 ± 111.52 c0.86 ± 0.03 d0.30 ± 0.02 bc
100.06 ± 0.00 ab271.27 ± 18.11 bc374.89 ± 0.52 b73.47 ± 1.01 bc1611.54 ± 22.44 bc0.89 ± 0.02 cd0.31 ± 0.03 bc
200.06 ± 0.00 ab303.07 ± 35.92 ab380.99 ± 1.86 b76.90 ± 2.18 b1727.08 ± 18.69 ab0.97 ± 0.02 bc0.31 ± 0.00 bc
500.06 ± 0.01 ab329.47 ± 29.82 ab400.34 ± 6.99 a91.83 ± 2.47 a1773.66 ± 5.47 ab1.03 ± 0.03 b0.37 ± 0.02 ab
1000.07 ± 0.00 a392.84 ± 21.67 a406.53 ± 10.39 a96.31 ± 0.41 a1952.15 ± 111.35 a1.18 ± 0.01 a0.41 ± 0.01 a
Note: Data are presented as the mean values ± standard error (n = 5). Different lowercase letters indicate significant differences between treatments at p < 0.05.
Table 4. Cadmium accumulation characteristics on dry base of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations.
Table 4. Cadmium accumulation characteristics on dry base of Cunninghamia lanceolata (Lambert) Hooker seedlings at different soil Cd concentrations.
Concentration of Cd
mg kg−1 DW		Cd Content in Leaves
mg kg−1 DW		Cd Content in Stems
mg kg−1 DW		Cd Content in Roots
mg kg−1 DW		Cd Content in Shoots
mg kg−1 DW		Remnant Cd Content in Soil
mg kg−1 DW		Plant BCFRoot BCFShoot BCFTF
51.49 ± 0.22 c4.18 ± 0.28 c40.19 ± 4.47 c2.71 ± 0.38 c3.11 ± 0.20 d3.34 ± 0.62 b8.04 ± 0.89 b0.54 ± 0.04 bc0.07 ± 0.00 a
103.02 ± 0.26 c10.20 ± 2.85 c89.16 ± 4.74 c6.18 ± 2.21 c5.70 ± 0.36 d3.52 ± 0.17 b8.92 ± 0.47 ab0.62 ± 0.13 bc0.07 ± 0.01 a
207.88 ± 0.36 c12.62 ± 1.18 c120.29 ± 7.45 c10.08 ± 1.25 c11.38 ± 0.69 c2.47 ± 0.02 b6.01 ± 0.37 b0.50 ± 0.04 c0.08 ± 0.01 a
5034.50 ± 4.88 b88.85 ± 9.46 b564.29 ± 67.32 b58.34 ± 9.48 b32.59 ± 2.67 b4.77 ± 0.31 a11.29 ± 1.35 a1.17 ± 0.11 a0.11 ± 0.01 a
10051.19 ± 3.69 a119.83 ± 10.86 a832.64 ± 112.23 a78.80 ± 10.17 a65.35 ± 3.42 a3.50 ± 0.44 b8.33 ± 1.12 ab0.79 ± 0.06 b0.10 ± 0.02 a
Note: Data are presented as the mean values ± standard error (n = 5). Different lowercase letters indicate significant differences between treatments at p < 0.05.
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Dai, D.; Hu, H.; Wen, J.; Chen, H.; Chen, G.; Cui, X. Cunninghamia lanceolata (Lambert) Hooker: A Promising Candidate for Phytoremediation of Cd-Contaminated Soils. Forests 2024, 15, 115. https://doi.org/10.3390/f15010115

AMA Style

Dai D, Hu H, Wen J, Chen H, Chen G, Cui X. Cunninghamia lanceolata (Lambert) Hooker: A Promising Candidate for Phytoremediation of Cd-Contaminated Soils. Forests. 2024; 15(1):115. https://doi.org/10.3390/f15010115

Chicago/Turabian Style

Dai, Dachuan, Hongling Hu, Jing Wen, Hong Chen, Gang Chen, and Xinglei Cui. 2024. "Cunninghamia lanceolata (Lambert) Hooker: A Promising Candidate for Phytoremediation of Cd-Contaminated Soils" Forests 15, no. 1: 115. https://doi.org/10.3390/f15010115

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