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Article

Alterations of Amino Acid Concentrations and Photosynthetic Indices in Light Irradiated Arabidopsis thaliana during Phytoextraction

by
Yanmei Chen
1,
Longfei Liang
2,
Dan Chen
1,
Tian Gan
3,
Min Cao
4 and
Jie Luo
1,*
1
College of Resources and Environment, Yangtze University, Wuhan 430100, China
2
Geophysical Exploration Brigade of Hubei Geological Bureau, Wuhan 430056, China
3
School of Civil Engineering, Shandong University, Jinan 250100, China
4
College of Natural Sciences, University of Leicester, University Road, Leicester LE1 7RH, UK
*
Author to whom correspondence should be addressed.
Sustainability 2021, 13(14), 7720; https://doi.org/10.3390/su13147720
Submission received: 22 June 2021 / Revised: 7 July 2021 / Accepted: 8 July 2021 / Published: 10 July 2021
(This article belongs to the Collection Risk Assessment and Management)
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Abstract

:
Hyperaccumulation of heavy metals is substantial in some hyperaccumulators; however, few studies have been conducted to reveal the effect of light irradiation on the variations of representative amino acids and photosynthetic indices, which can represent the antioxidant capacity of plants during phytoremediation. The physiochemical responses of Arabidopsis thaliana to Cd stress were compared during six light irradiation treatments. The results of the experiment showed that the stress adaptation of A. thaliana was enhanced in all light irradiation treatments, except for monochromatic blue-light irradiation. The concentrations of glutamic acid and glutamine decreased significantly in pure blue light compared with the other treatments. The decrease in the concentrations of these two amino acids might be induced by an intensive biosynthesis of defensive factors, as manifested in the declined photosynthetic indices. Concentrations of aspartic acid and asparagine involved in the ammonification, absorption, and transportation of nitrogen in vascular plants increased in the red and blue combined irradiation treatments compared with the control, corresponding to the improved photosynthetic capacity of the species. The concentration of proline, which can represent environmental stresses including metal toxicity and excessive light energy, generally increased with an increasing ratio of blue light. This study proposes the key roles of amino acids and photosynthetic indices in light-motivated Cd pollution responses in A. thaliana.

1. Introduction

With the rapid development of the economy and society, environmental contamination has become increasingly severe. Soil pollution has gained worldwide concern because soil is an important non-renewable resource that provides habitats for terrestrial creatures and a medium for crop cultivation. Cd is regarded as one of the most toxic heavy metals to plants and animals owing to its high bioavailability and toxicity [1]. Approximately 30 million kilogram of Cd is discharged into environmental media annually, with an estimated 13 million kilograms released from anthropogenic activities [2]. Electronic waste (e-waste) recycling is one of the most environmentally harmful anthropogenic activities. The contaminated soils treated in the present study were sampled from an e-waste disassembling and recycling town located in southern China. A large area of soils in the town has been polluted by disassembling activities owing to primitive dismantling methods [3]. Environmentally harmful businesses have deleterious effects on the health of the local inhabitants, especially infants and children. For example, Cai et al. (2019) [4] found that metal exposure in Guiyu resulted in an increase in child sensory integration difficulties, compared with a nearby town not involved in the disassembling business. Therefore, it is necessary to develop an environmentally friendly and economically viable method for decontaminating Cd-polluted fields, especially agricultural land.
The use of green plants, including hyperaccumulators and high-biomass-generating plants to stabilize or remove pollutants in soils, a technology called phytoremediation, is a developing feasible method for in situ decontamination [5,6]. Plants are used to extract metals from substrates and migrate them to aerial parts (phytoextraction) or to decrease their activity and toxicity in soils (phytostabilization). Both phytoextraction and phytostabilization should allow plants to accumulate as many metals as they can improve the remediation effect.
When Cd enters plant cells, it can cause changes in numerous biochemical processes at the cellular and subcellular levels by decreasing enzymatic activities, disturbing the functional groups of metabolites, replacing nutrients, and damaging membrane integrity [7]. Damaged cells cannot perform their physiological functions normally, thereby obstructing the conducting system and diminishing photosynthetic efficiency, resulting in considerable deleterious effects on the health of plant tissues [8,9].
In response to stress induced by excessive Cd, plants have developed multiple adaptation mechanisms to protect cells, such as activating signal transduction processes and biosynthesizing more proteins and pigments with antioxidant capacity in the impaired organ [5,10]. However, energy consumption processes require higher photosynthetic efficiency and perturb the normal physiological functions of the plants [11]. As precursors for protein biosynthesis, amino acids play a key role in the development and metabolic processes of plants. It has been reported that plants that accumulate large quantities of heavy metals are associated with a substantial accumulation of free amino acids [12]. In addition, amino acids are involved in the biosynthesis of phytochelatin, which can decrease the biological activity of metals by forming stable metal–chelate complexes [13].
Photosynthetic indices have been proven to be especially sensitive to Cd, which can decrease the photosynthetic efficiency of the photosynthetic apparatus by disturbing electron transportation, breaking CO2 fixation, and resulting in stomatal closure [14]. Therefore, observations of photosynthetic indices are a nondestructive and sensitive technology for estimating the health conditions of plants [8,15]. Furthermore, the weakening of the photosynthetic efficiency leads to a decline in the replenishment of metabolic energy for N absorption and ammonification, disturbing the synthesis of amino acids [16]; thus, the relationship between amino acids and photosynthetic indices should be revealed during phytoremediation.
Light is an essential natural resource for modulating the germination, sprouting, flowering, and bearing fruit of plants. At the molecular level, light acts as an energy source and is involved in the biosynthesis of chlorophyll, carotenoids, and amino acids [17]. In addition, as a signaling source, light can regulate apical dominance through cryptochrome and phytochrome, respectively [18]. At the macro level, the utilization of light in agronomy and horticulture has become increasingly popular because it is a physical trigger in plants rather than a chemical trigger. Alterations in the morphology and function of plant tissues have been reported owing to changes in light quantity, quality, and duration, and these alterations have been shown to be species-specific. For instance, Li et al. (2010) [19] suggested that blue light significantly increased the chlorophyll level, leaf thickness, palisade parenchyma length, and stomatal area of Gossypium hirsutum compared with the control, while Zou et al. (2020) [20] reported that blue light decreased the growth rate, root length, and photosynthetic efficiency of A. thaliana. Our previous work also found that a proper blue/red light ratio can increase the Cd removal efficiency of Noccaea caerulescens by simultaneously enhancing its metal uptake capacity and oxidation resistance [21].
Arabidopsis thaliana has become a popular plant for the analysis of metal accumulation and decontamination [22,23]. However, reports on the roles and interrelation of amino acids and photosynthetic indices in the phytoremediation of Cd by A. thaliana under different light irradiation treatments are limited. It is safe to hypothesize that different light irradiation treatments would result in different physiological responses of plants to environmental stresses, including Cd pollution. The current study aims to estimate the influences of different light treatments on biomass yield and Cd extraction capacity of A. thaliana, assess variations in the accumulation of amino acids and photosynthetic indices in the species under different light treatments, and reveal the resistance of the species to Cd stress by focusing on its micro indices.

2. Materials and Methods

2.1. Soil and Plant

Seeds of A. thaliana (wild-type) were sampled from a metalliferous field and cultivated according to the process conducted by Szopiński et al. (2019) [24]. Briefly, after being sterilized using 50% ethanol, the seeds were germinated in disinfected pots filled with vermiculite after further light irradiation treatments.
Considering the geochemical background and topography of the study region, 200 topsoil samples (0−20 cm) were collected. The air-dried and sieved (2-mm mesh) samples were blended to obtain a composite substrate. The blended substrate was equilibrated by four saturating and drying processes to obtain a homogeneous distribution of the metal. After equilibration, the substrate was divided into approximately 6000 g aliquots and filled in disinfected pots for A. thaliana transplantation.

2.2. Light Irradiation Treatment

After 3 weeks of acclimation, 10 seedlings were transplanted to each pot and thinned to five before light illumination. Six light irradiation treatments with five replications, including monochromatic blue (B100), 25% red and 75% blue (B75), 50% red and 50% blue (B50), 90% red and 10% blue (B10), and monochromatic red (B0), as well as an incandescent lamp (control), were conducted under controlled conditions (22 °C, 60% relative humidity). The illumination intensities were set at 200 μmol·m−2·s−1 photosynthetic photon flux density at an 8 h·night/16 h·day photoperiod, and a spectrometer was used to monitor the constancy of light illumination. Four weeks after light irradiation, all seedlings were harvested and divided into roots and shoots. The plant tissues were cleaned by running water to remove foreign materials and soaked in 10 mM EDTA to eliminate the adsorbed ions.

2.3. Cd Analysis and Quality Control

For the analysis of Cd, dried soil and plant samples were pulverized and sieved by 74-μm meshes. The powders were digested using aqua regia at 120 °C for 6 h and then diluted with deionized water [25]. After cooling, the digestion was filtered via a 0.45-µm membrane, and the concentration of Cd in the filtrate was quantified by ICP-MS (Agilent 7700, Santa Clara, CA, USA). An Agilent multi-element calibration standard (Agilent, ZCA-8500-6940) was applied to each measurement batch for quality control. The reference material GBW10010 (plant) was also analyzed for quality assurance.
The content of soil Cd (3.83 ± 0.46 mg kg−1) was only analyzed at the beginning of the treatment because the duration of this experiment was not long enough for A. thaliana to change the pseudototal Cd content. The phytoremediation efficiency of the species was evaluated based on its biomass generation and Cd uptake capacity.

2.4. Measurement of Chlorophyll Fluorescence

A fluorometer (PAM 2100, WALZ Corporation, Forchheim, Germany) was used to measure the chlorophyll fluorescence. Minimal (F0) and maximal (FM) fluorescence were measured using a saturating flash after a 30 min dark adaptation, and then the plant leaves were illuminated using an actinic light for F′ (steady state fluorescence level in light-adapted tissues) and F′M (maximal chlorophyll fluorescence in light-adapted tissues) measurements according to the process performed by Li et al. (2015) [26]. The chlorophyll fluorescence parameters, including maximum quantum yield of photosystem II (PSII) after dark adaptation of (Fv/FM), effective quantum yield of PSII (Y(II)), photochemical quenching (qP), and non-photochemical quenching (NPQ) were calculated according to Agrawal et al. (2016) [27].

2.5. Measurement of MDA, H2O2

MDA was determined according to the process described by Zhang et al. (2019) [28]. Briefly, the plant leaves (0.5 g) were homogenized in an 8 mL thiobarbituric acid (TBA, 10%) solution. After centrifugation at 4000× g for 20 min, the mixture of the filtrate (2 mL) and TBA (2 mL, 0.6%) was boiled for 30 min. After cooling, the absorbance of the solution was determined at 532, 450, and 600 nm to calculate the MDA content using the following formula:
MDA = 6.45 × (A532 − A600) − 0.56 × A450
Fresh leaves (0.1 g) were homogenized in acetone (1 mL), and then a hydrogen peroxide assay kit (BC3595, Solarbio, Beijing, China) was used to determine the concentration of H2O2 in the plant leaves. The measurements were performed according to the manufacturer’ s instructions.

2.6. Measurement of Amino Acids

The plant tissues were pretreated according to the method suggested by Xu and Xiao (2016) [29] for chromatographic analysis. In brief, 0.15 g of the plant samples was shaken in 1.8 mL trifluoroacetic acid (10% v/v) for 5 min. After ultrasonic treatment for 5 min, the solution was centrifuged at 12,000 rpm for 15 min. After filtration, the residue was extracted using the same procedure, and the recovered supernatants were combined to improve the precision of the analysis. The combined solution was filtered by a 0.2 μm polycarbonate membrane (Whatman, Maidstone, UK) and then analyzed using a high-performance liquid chromatograph (HPLC, Agilent 1200, Santa Clara, CA, USA). Five amino acids, including glutamic acid (Glu), glutamine (Gln), aspartic acid (Asp), asparagine (Asn), and proline (Pro), were measured.

2.7. Statistical Analysis

All the data in this study are shown as the average values of five replicates. The influence of light irradiation treatments on the dry weight, Cd concentration, chlorophyll fluorescence parameters, pigment levels, and amino acid levels were determined using one-way analysis of variance. Comparisons of means were performed by Fisher’s LSD post-hoc tests at 0.05 probability. The statistical analysis of data was executed using SPSS 15.0.

3. Results and Discussion

3.1. Plant Growth

The dry weight of A. thaliana in the current experiment ranged from 0.40 to 1.32 g, which was slightly lower than the values recorded in previous studies [30,31]. Light irradiation significantly enhanced the biomass of the plant roots compared with the control, except for monochromatic blue light, which resulted in the lowest value at the termination of the treatment (Figure 1). There was a proportional decrease in the dry weight of the plant roots with increasing ratios of blue light, except for B10, which triggered the highest value. All the light treatments enhanced the biomass yield of the above ground parts of A. thaliana compared with the control during the experiment, and the highest value was observed in B10. As shown in Figure 1, B0 had a lower aerial part to whole plant ratio than the control, while other treatments had higher ratios. In general, the dry weight of the aerial parts increased with an increase in the ratio of blue light until it reached a peak of 1.03 g in B50.

3.2. Cd Content

As a Cd accumulator, A. thaliana can accumulate significantly higher levels of the metal in its aerial parts (generally higher than 100 mg·kg−1) relative to the rhizosphere soil [32]. Compared with previous treatments that grew the species in a sewage sludge applied soil [31], or a Cd-spiked substrate [33], in the current experiment, A. thaliana in the control had significantly lower Cd levels in its aerial parts, which did not achieve the criterion of 100 mg·kg−1 for Cd.
Light irradiation treatments changed the Cd content in the plant roots and shoots. There was a decline in the Cd concentrations in the plant roots with increasing doses of blue light. Relative to the control, all treatments increased the content of Cd in the plant shoots, except for B0, which declined the value significantly. The concentrations of Cd in the plant shoots elevated with enhancing ratios of blue light until it achieved a peak of 121.6 mg·kg−1 in B50, after which the metal in the aerial parts declined significantly (Figure 2). Notably, in B10, B50, and B75, the concentrations of Cd in the aerial parts of A. thaliana met the criterion of a Cd hyperaccumulator.
The translocation factor (TF), calculated by dividing the content of Cd in the aerial parts by that in the roots, was used to assess the Cd migration and accumulation ability of the species [34]. The TF values in the control, B0, B10, B50, B75, and B100 were 9.1, 5.0, 9.2, 11.2, 11.4, and 12.3, respectively. The results indicated that monochromatic red light drove A. thaliana to translocate more Cd into its roots, while blue light had the opposite effect.

3.3. MDA and H2O2 Content

Both heavy metals and excessive illumination can induce the generation and accumulation of superoxide radicals [35,36]. In the present study, the accumulation of H2O2 in the plant tissues was measured to estimate the level of oxidative damage under various treatments. As shown in Figure 3, the levels of H2O2 in the above ground parts of A. thaliana elevated with enhancing ratios of blue light. Relative to the control, three red–blue combinations (B10, B50, and B75) increased the concentrations of H2O2 slightly (p > 0.05), while monochromatic red and blue light caused a decrease and increase, respectively. The accumulation of H2O2 did not correlate well with the variation in Cd content (r = 0.5, p = 0.3). For instance, the highest H2O2 was recorded in B100, in which the content of Cd in plant shoots was similar to that of the control. These results indicate that Cd accumulation might not be a unique mechanism for the increased H2O2 concentration observed in this study.
MDA is regarded as an effective indicator of lipid peroxidation [37]. Except for B100, which had the highest MDA content, the levels of MDA in the plant shoots elevated with enhancing ratios of blue light until it achieved a peak at B50 (Figure 3). Relative to the control, all treatments increased the level of MDA in the above ground parts of A. thaliana, except for monochromatic red light. The positive correlation between MDA and Cd content was also not significant (r = 0.6, p = 0.2).

3.4. Chlorophyll Fluorescence Characteristic

Chlorophyll fluorescence parameters can reflect the status and properties of photosynthetic processes with variations in light assimilation, redistribution, divergence, and conversion [38].
As shown in Figure 4, Fv/FM, which is regarded as a dependable indicator of photoinhibition, showed no significant difference in all treatments. However, a clear trend that Fv/FM elevated with enhancing doses of blue light until it achieved a peak at B75, after which the lowest value among all treatments was observed in B100. A decrease in Fv/FM implies a decrease in the maximum quantum yield of an open photosynthetic system II (PSII), as well as an increase in light dissipation, indicating damage to the reaction center [39]. All the light treatments, except B100, had no significant effect on Y(II). The combination of red and blue light increased Y(II) in a variation from 3.0% to 14.5%, and the monochromatic blue light decreased Y(II) significantly by 33.1% compared with the control. The recorded decrease in Y(II) indicates that monochromatic blue light aggravated the light energy dissipation of the antenna pigment and resulted in a decline in the efficiency of excited energy trapped by PSII [40].
All the light irradiation treatments had no significant effect on qP, and the lowest qP was observed in B100. NPQ gradually decreased in contrast to the increase in qP, and monochromatic blue light increased NPQ by 57.8%, 131.5%, 61.7%, 50.0%, and 14.6% relative to the control, B0, B10, B50, and B75, respectively. Considerable amounts of the captured light are used to facilitate photosynthesis (qP) or are dissipated as nonradiative heat (NPQ). It is a protective mechanism of the photosynthetic system that may minimize the oxidative damage induced by excessive illumination [35,41].

3.5. Amino Acid

The results of the experiment suggested different influences of light irradiation on the amino acid concentrations. The concentration of Glu in the aerial parts of A. thaliana increased slightly in B0, but other treatments significantly decreased the concentration (Table 1). Except for monochromatic red, all the light irradiation treatments decreased the content of Gln compared with the control.
Asp and Asn, which are formed by Gln and Glu, translocate organic N from the source to sink in plants. Our results demonstrated that the content of Asp raised with the enhancing ratio of blue light until it achieved a peak at B50, after which the concentration decreased significantly (Table 1). The variation trend of Asn was similar to that of Asp, but the highest content was observed in B10.
Pro is a reliable diagnostic indicator of different abiotic stresses, including Cd toxicity [42] and light illumination [43]. In the current study, the levels of Pro were significantly higher in B50, which had the highest Cd content in the aerial parts of A. thaliana, and B100, which accepted the monochromatic blue light.

3.6. Phytoremediation Efficiency

The difference in the initial soil Cd concentration and the acceptable threshold (0.3 mg·kg−1) multiplied by the weight of the soil (6 kg per pot) was the amount of the metal that needed to be removed. The Cd accumulation capacity (AC) of A. thaliana was calculated as the product of its dry weight and Cd content. The necessary growing cycles to decontaminate the soil were calculated as the quotient of the excess Cd and the AC divided by five. According to the biomass generation and Cd accumulation capacity of A. thaliana, the AC of the species were 0.13, 0.30, 0.57, 0.64, 0.26, and 0.15 mg Cd per pot in the control, B0, B10, B50, B75, and B100, respectively. Therefore, 168, 72, 38, 33, 80, and 142 growing cycles are required for the species to clean the soil under the corresponding treatments. Obviously, B50, which reduced the required time by 80% compared with the control, was the optimal strategy.
As shown in Figure 1, the highest dry weight of A. thaliana was not observed in B50, but the relatively higher Cd extraction ability of the species counteracted the reduction in biomass. However, both the biomass yield and metal extraction ability of A. thaliana decreased with the increasing proportion of blue light, reducing the phytoremediation efficiency of the species.

4. Discussion

4.1. Responses of Biomass Yield and Cd Accumulation to Light Irradiation

The responses of plant species to light illumination are specific to species. Lin et al. (2013) [44] found that monochromatic red LED increased the fresh and dry weight of Lactuca sativa significantly when compared with the control, in agreement with the results of our study. In contrast, our previous study suggested that red light increased the root dry weight of Noccaea caerulescens, but decreased its leaf biomass, and the improved root biomass could not offset the reduction in the leaf biomass [21]. Interestingly, the present study found that although monochromatic blue light resulted in the lowest dry weight of roots and aerial parts of A. thaliana, the application of a small quantity of blue light can significantly enhance the biomass generation capacity of the species, as manifested in the highest biomass of A. thaliana in B10. This finding agrees with the reports of Hogewoning et al. (2010) [45] who found that only 7% blue light was sufficient to prevent any overt dysfunctional photosynthesis of Cucumis sativus.
To reveal the effect of illumination on plant health at the cellular level, Dong et al. (2014) [46] reported that a single light might induce a burst of reactive oxygen, resulting in a surge in superoxide radicals, which would induce oxidative damage to cell membranes. However, in the presence of heavy metals, the physiological responses of plants will become more complex. Suitable light irradiation can cause plants to accumulate more metals, which would have deleterious effects on plant cells [47]; therefore, the variation in the Cd concentration in the plant tissues under different light treatments was examined.

4.2. Influences of Light Irradiation on Cd Accumulation

The primary toxic mechanisms of Cd on plant cells are the reduction of glutathione, inhibition of protein synthesis, and substitution of pivotal elements, including Zn and Mg, in the chloroplasts [48]. Therefore, more energy is consumed to counteract the detrimental effects caused by Cd, resulting in the redistribution of nutrients and disturbing the normal function of the plant organs. Light irradiation treatments generally increased Cd content in the roots and the above ground parts of A. thaliana, but there was a weak positive correlation between the Cd content and plant dry weight (r = 0.7, p = 0.08), indicating that a suitable light treatment might alleviate the negative effects of Cd on plant health.
The impacts of light quantity, quality, and duration on nutrient cycling in plant tissues have been fully reported, but the uptake and translocation of pollutants including Cd in the soil and plant under the impact of illumination have rarely been revealed. To date, only Kwon et al. (2017) [49] have studied the influence of light irradiation (red, blue, yellow, and their combination) on the adsorption and absorption of Cu and Zn by microalgae and reported that microalgae grown under monochromatic red light had the highest Cu and Zn decontamination efficiency. However, the physiological response of algae to light might differ from that of plants. It has been suggested that the transpiration rate of plants can influence the metal uptake capacity of plants. For instance, Wan et al. (2015) [50] evaluated the role of transpiration in the extraction of As from the perspective of transpiration modulation and found that Pteris vittata grown in a humid environment had a 40% higher transpiration rate and 40% higher leaf As level compared with plants grown in dry habitats. Light irradiation can influence the transpiration rate of plants by affecting their photosynthetic system; therefore, the influences of light treatment on oxidative damage photosynthetic indices were discussed.

4.3. Relationship among Oxidative Damage, Photosynthetic Indices, and Amino Acid Content

It has been reported that the accumulation of pollutants, including metals, in plant tissues results in oxidative damage by promoting the generation of reactive oxygen species, which have deleterious effects on the cell membrane [51,52,53]. However, the increase in H2O2 and MDA was not significantly related to the extraction and accumulation of the metal in A. thaliana. In general, the pollutant uptake and biomass generation contradict each other. The contradictory results found in this study could be supported by Wu et al. (2018) [54], who reported that the biomass of Malva crispa, Celosia argentea, and Celosia cristata did not decline as the Cd content increased, and it was even higher than that of the control. They attributed low-dose promotion to the hormetic dose responses. A minute dose of Cd can increase the growth rate of some plants by activating antioxidant enzymes and hormones in the plant tissues. In addition, light illumination itself can impact the health of plants by modulating the electron transport rate and photochemical quenching of the photosystems. Therefore, variations in amino acid and chlorophyll fluorescence parameters are discussed. It is worth noting that cell death in A. thaliana can be regulated by apoplastic ROS and jasmonic acid [55], and cell death in the species under different light treatments should be revealed in future.
Combining the result that a relatively low Cd content in the aerial parts of A. thaliana was recorded in B100, the decreased qP and increased NPQ indicated that monochromatic blue light induced photo-oxidative damage to the photosynthetic apparatus, and a defense mechanism was activated to alleviate the damage. This finding is inconsistent with the results of Li et al. (2017) [56], who found that qP and NPQ of wheat under ultraviolet light (UV-B) stress declined significantly compared with the control. This might be because the oversupplied energy provided by ultraviolet light can damage the self-protecting ability of the PSII reaction centers because their maximum capacity is overwhelmed. This suggests that monochromatic blue light does not overwhelm the self-protecting ability of PSII in A. thaliana.
Considering the result of MDA in H2O2 concentrations in plant tissues, the oxidative damage in A. thaliana was mainly induced by monochromatic blue light irradiation, rather than the accumulated Cd. In contrast, in B10, B50, and B75, oxidative damage may have been induced by the concentration of Cd.
The reduction in the Glu content might be induced by intensive biosynthesis of defense elicitors, which require more energy. Gln, which can represent the N utilization pathway, is one of the dominant amino acids in A. thaliana. Gln is a donor catalyzed by glutamate synthase, which is a key enzyme in the assimilation of inorganic N [57]. This process represents the energy status of the photosynthetic apparatus. Aspartate aminotransferase controls the biosynthesis of Asp, and its activity is sensitive to environmental stresses [58]. The significantly greater reduction in the Asp concentration in B100 indicates increased stress under the monochromatic blue light treatment. Both the Cd accumulation and the increasing ratio of blue light (when higher than 50%) induced negative effects on the synthesis of Asn. Considering the variation trends of amino acids associated with the accumulation of Cd and light irradiation treatments, we hypothesized that monochromatic blue light could induce greater damage to the photosynthetic system of A. thaliana than Cd. This hypothesis should be verified through more sophisticated experiments.

5. Conclusions

The results of this experiment demonstrate that the phytoremediation efficiency of A. thaliana could benefit from combinations of blue and red light, especially B10 and B50, which resulted in better biomass generation and Cd accumulation capacity. Monochromatic blue light induced significantly lower biomass and Cd content of A. thaliana compared with other light irradiation treatments, although it enhanced the phytoextraction ability of the species relative to the control. As a high-energy light, blue light induced photoinhibition in the plant leaves, as manifested by the decreased photosynthetic indices, including Fv/FM, Y(II), and qP in B100. However, the significantly higher NPQ in B100 compared with other light irradiation treatments indicates that the photosynthetic system can dissipate excessive light energy as heat to alleviate continuous oxidative damage. In other words, blue light did not overwhelm the self-protecting ability of the species. The variations in amino acid concentrations suggest that both Cd accumulation and a high ratio of blue light could trigger deleterious effects on A. thaliana, thus decreasing its phytoremediation efficiency. In addition, the continuous depletion of stratospheric O3 could result in an increase in ultraviolet light, which contains significantly more energy compared with blue light in the near surface, and the effects of ultraviolet light on the phytoremediation efficiency of plants should be studied in future research. Cell death and other ROS including superoxide and hydroxyl radicals, which can also reflect the physiological responses of plants to external environments will be measured in our future work.

Author Contributions

Conceptualization, J.L.; methodology, J.L. and Y.C.; software, D.C. and T.G.; validation, Y.C. and L.L.; formal analysis, J.L. and D.C.; investigation, L.L. and T.G.; resources, J.L. and Y.C.; data curation, M.C.; writing—original draft preparation, Y.C. and J.L.; writing—review and editing, M.C. and T.G.; visualization, Y.C. and M.C.; supervision, J.L.; project administration, J.L.; funding acquisition, J.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the National Natural Science Foundation of China, grant number 21876014 and the Natural Science Foundation of Hubei Province of China, grant number 2018CFB258.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Ehsan, S.; Ali, S.; Noureen, S.; Mahmood, K.; Farid, M.; Ishaque, W.; Shakoor, M.B.; Rizwan, M. Citric acid assisted phytoremediation of cadmium by Brassica napus L. Ecotoxicol. Environ. Saf. 2014, 106, 164–172. [Google Scholar] [CrossRef]
  2. Gallego, S.M.; Pena, L.B.; Barcia, R.A.; Azpilicueta, C.E.; Iannone, M.F.; Rosales, E.P.; Zawoznik, M.S.; Groppa, M.D.; Benavides, M.P. Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environ. Exp. Bot. 2012, 83, 33–46. [Google Scholar] [CrossRef]
  3. Wu, Q.; Du, Y.; Huang, Z.; Gu, J.; Leung, J.Y.S.; Mai, B.; Xiao, T.; Liu, W.; Fu, J. Vertical profile of soil/sediment pollution and microbial community change by e-waste recycling operation. Sci. Total Environ. 2019, 669, 1001–1010. [Google Scholar] [CrossRef] [PubMed]
  4. Cai, H.; Xu, X.; Zhang, Y.; Cong, X.; Lu, X.; Huo, X. Elevated lead levels from e-waste exposure are linked to sensory integration difficulties in preschool children. Neuro Toxicol. 2019, 71, 150–158. [Google Scholar] [CrossRef] [PubMed]
  5. Ullah, A.; Mushtaq, H.; Ali, H.; Munis, M.F.H.; Javed, M.T.; Chaudhary, H.J. Diazotrophs-assisted phytoremediation of heavy metals: A novel approach. Environ. Sci. Pollut. Res. 2015, 22, 2505–2514. [Google Scholar] [CrossRef] [PubMed]
  6. Niñerola, V.B.; Navarro-Pedreño, J.; Lucas, I.G.; Pastor, I.M.; Vidal, M.M.J. Geostatistical assessment of soil salinity and cropping systems used as soil phytoremediation strategy. J. Geochem. Explor. 2017, 174, 53–58. [Google Scholar] [CrossRef]
  7. Guo, Q.; Meng, L.; Zhang, Y.N.; Mao, P.C.; Tian, X.X.; Li, S.S.; Zhang, L. Antioxidative systems, metal ion homeostasis and cadmium distribution in Iris lactea exposed to cadmium stress. Ecotoxicol. Environ. Saf. 2017, 139, 50–55. [Google Scholar] [CrossRef]
  8. Paunov, M.; Koleva, L.; Vassilev, A.; Vangronsveld, J.; Goltsev, V. Effects of different metals on photosynthesis: Cadmium and zinc affect chlorophyll fluorescence in durum wheat. Int. J. Mol. Sci. 2018, 19, 787. [Google Scholar] [CrossRef] [Green Version]
  9. Arena, C.; Figlioli, F.; Sorrentino, M.C.; Izzo, L.G.; Capozzi, F.; Giordano, S.; Spagnuolo, V. Ultrastructural, protein and photosynthetic alterations induced by Pb and Cd in Cynara cardunculus L., and its potential for phytoremediation. Ecotoxicol. Environ. Saf. 2017, 145, 83–89. [Google Scholar] [CrossRef]
  10. Gupta, D.K.; Tripathi, R.D.; Rai, U.N.; Dwivedi, S.; Mishra, S.; Srivastava, S.; Inouhe, M. Changes in amino acid profile and metal content in seeds of Cicer arietinum L. (chickpea) grown under various fly-ash amendments. Chemosphere 2006, 65, 939–945. [Google Scholar] [CrossRef]
  11. Lanoue, J.; Leonardos, E.D.; Grodzinski, B. Effects of Light Quality and Intensity on Diurnal Patterns and Rates of Photo-Assimilate Translocation and Transpiration in Tomato Leaves. Front. Plant Sci. 2018, 9, 1–14. [Google Scholar] [CrossRef] [Green Version]
  12. Zhu, G.; Xiao, H.; Guo, Q.; Zhang, Z.; Zhao, J.; Yang, D. Effects of cadmium stress on growth and amino acid metabolism in two Compositae plants. Ecotoxicol. Environ. Saf. 2018, 158, 300–308. [Google Scholar] [CrossRef] [PubMed]
  13. Wu, J.; Chen, A.; Peng, S.; Wei, Z.; Liu, G. Identification and application of amino acids as chelators in phytoremediation of rare earth elements lanthanum and yttrium. Plant Soil 2013, 373, 329–338. [Google Scholar] [CrossRef]
  14. Bayçu, G.; Moustaka, J.; Gevrek, N.; Moustakas, M. Chlorophyll Fluorescence Imaging Analysis for Elucidating the Mechanism of Photosystem II Acclimation to Cadmium Exposure in the Hyperaccumulating Plant Noccaea caerulescens. Materials 2018, 11, 2580. [Google Scholar] [CrossRef] [Green Version]
  15. Jan, L.; Fefer, D.; Košmelj, K.; Gaberščik, A.; Jerman, I. Geomagnetic and strong static magnetic field effects on growth and chlorophyll a fluorescence in Lemna minor. Bioelectromagnetics 2015, 36, 190–203. [Google Scholar] [CrossRef]
  16. Tripathi, R.D.; Singh, R.; Tripathi, P.; Dwivedi, S.; Chauhan, R.; Adhikari, B.; Trivedi, P.K. Arsenic accumulation and tolerance in rootless macrophyte Najas indica are mediated through antioxidants, amino acids and phytochelatins. Aquat. Toxicol. 2014, 157, 70–80. [Google Scholar] [CrossRef] [PubMed]
  17. Chen, B.; Zou, D.; Zhu, M.; Yang, Y. Effects of CO2 levels and light intensities on growth and amino acid contents in red seaweed Gracilaria lemaneiformis. Aquac. Res. 2017, 48, 2683–2690. [Google Scholar] [CrossRef]
  18. Jeong, B.R.; Sivanesan, I. Impact of light quality and sucrose on adventitious shoot regeneration and bioactive compound accumulation in Ajuga multiflora Bunge. Sci. Hortic. 2018, 236, 222–228. [Google Scholar] [CrossRef]
  19. Li, H.; Xu, Z.; Tang, C. Effect of light-emitting diodes on growth and morphogenesis of upland cotton (Gossypium hirsutum L.) plantlets in vitro. Plant Cell Tissue Organ Cult. 2010, 103, 155–163. [Google Scholar] [CrossRef]
  20. Zou, T.; Wu, B.; Wu, W.; Ge, L.; Xu, Y. Effects of different spectra from LED on the growth, development and reproduction of Arabidopsis Thaliana. Phyton 2020, 89, 275–289. [Google Scholar] [CrossRef]
  21. Luo, J.; Cao, M.; Zhang, C.; Wu, J.; Gu, X.W.S. The in fluence of light combination on the physicochemical characteristics and enzymatic activity of soil with multi-metal pollution in phytoremediation. J. Hazard. Mater. 2020, 393, 1–10. [Google Scholar] [CrossRef]
  22. Vandenbrink, J.P.; Herranz, R.; Medina, F.J.; Edelmann, R.E.; Kiss, J.Z. A novel blue-light phototropic response is revealed in roots of Arabidopsis thaliana in microgravity. Planta 2016, 244, 1201–1215. [Google Scholar] [CrossRef]
  23. Lin, Y.F.; Hassan, Z.; Talukdar, S.; Schat, H.; Aarts, M.G.M. Expression of the Znt1 zinc transporter from the metal hyperaccumulator noccaea caerulescens confers enhanced zinc and cadmium tolerance and accumulation to Arabidopsis thaliana. PLoS ONE 2016, 11, e0149750. [Google Scholar] [CrossRef] [PubMed]
  24. Szopiński, M.; Sitko, K.; Gieroń, Ż.; Rusinowski, S.; Corso, M.; Hermans, C.; Verbruggen, N.; Małkowski, E. Toxic effects of cd and zn on the photosynthetic apparatus of the Arabidopsis halleri and Arabidopsis arenosa pseudo-metallophytes. Front. Plant Sci. 2019, 10, 1–13. [Google Scholar] [CrossRef] [Green Version]
  25. Ok, Y.S.; Kim, S.C.; Kim, D.K.; Skousen, J.G.; Lee, J.S.; Cheong, Y.W.; Kim, S.J.; Yang, J.E. Ameliorants to immobilize Cd in rice paddy soils contaminated by abandoned metal mines in Korea. Environ. Geochem. Health 2011, 33, 23–30. [Google Scholar] [CrossRef] [PubMed]
  26. Li, S.; Yang, W.; Yang, T.; Chen, Y.; Ni, W. Effects of Cadmium Stress on Leaf Chlorophyll Fluorescence and Photosynthesis of Elsholtzia argyi—A Cadmium Accumulating Plant. Int. J. Phytoremed. 2015, 17, 85–92. [Google Scholar] [CrossRef]
  27. Agrawal, D.; Allakhverdiev, S.I.; Jajoo, A. Cyclic electron flow plays an important role in protection of spinach leaves under high temperature stress. Физиoлoгия Растений 2016, 63, 225–230. [Google Scholar] [CrossRef]
  28. Zhang, X.H.; Liu, Y.H.; Liu, B.W.; Liu, Q.; Wen, S.Y.; Ao, B.; Lin, Z.Q.; Zheng, Y.L.; Yang, W.Z.; Chu, X.T.; et al. Arbuscular mycorrhiza fungus improved growth, antioxidant defense, and endogenous hormones in tall fescue under low-light stress. South Afr. J. Bot. 2019, 127, 43–50. [Google Scholar] [CrossRef]
  29. Xu, Y.; Xiao, H. Free amino acid concentrations and nitrogen isotope signatures in Pinus massoniana (Lamb.) needles of different ages for indicating atmospheric nitrogen deposition. Environ. Pollution. 2017, 221, 180–190. [Google Scholar] [CrossRef] [PubMed]
  30. Tlustoš, P.; Břendová, K.; Száková, J.; Najmanová, J.; Koubová, K. The long-term variation of Cd and Zn hyperaccumulation by Noccaea spp and Arabidopsis halleri plants in both pot and field conditions. Int. J. Phytoremed. 2016, 18, 110–115. [Google Scholar] [CrossRef]
  31. McGrath, S.P.; Lombi, E.; Gray, C.W.; Caille, N.; Dunham, S.J.; Zhao, F.J. Field evaluation of Cd and Zn phytoextraction potential by the hyperaccumulators Thlaspi caerulescens and Arabidopsis halleri. Environ. Pollut. 2006, 141, 115–125. [Google Scholar] [CrossRef] [PubMed]
  32. Li, J.T.; Gurajala, H.K.; Wu, L.H.; Van Der Ent, A.; Qiu, R.L.; Baker, A.J.M.; Tang, Y.T.; Yang, X.E.; Shu, W.S. Hyperaccumulator Plants from China: A Synthesis of the Current State of Knowledge. Environ. Sci. Technol. 2018, 52, 11980–11994. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  33. Tewes, L.J.; Stolpe, C.; Kerim, A.; Krämer, U.; Müller, C. Metal hyperaccumulation in the Brassicaceae species Arabidopsis halleri reduces camalexin induction after fungal pathogen attack. Environ. Exp. Bot. 2018, 153, 120–126. [Google Scholar] [CrossRef]
  34. Aghababaei, F.; Raiesi, F.; Hosseinpur, A. The significant contribution of mycorrhizal fungi and earthworms to maize protection and phytoremediation in Cd-polluted soils. Pedobiologia 2014, 57, 223–233. [Google Scholar] [CrossRef]
  35. Heber, U.; Bukhov, N.G.; Shuvalov, V.A.; Kobayashi, Y.; Lange, O.L. Protection of the photosynthetic apparatus against damage by excessive illumination in homoiohydric leaves and poikilohydric mosses and lichens. J. Exp. Bot. 2001, 52, 1999–2006. [Google Scholar] [CrossRef] [Green Version]
  36. Huang, M.; Ai, H.; Xu, X.; Chen, K.; Niu, H.; Zhu, H.; Sun, J.; Du, D.; Chen, L. Nitric oxide alleviates toxicity of hexavalent chromium on tall fescue and improves performance of photosystem II. Ecotoxicol. Environ. Saf. 2018, 164, 32–40. [Google Scholar] [CrossRef]
  37. Fatima, A.; Singh, A.A.; Mukherjee, A.; Agrawal, M.; Agrawal, S.B. Variability in defence mechanism operating in three wheat cultivars having different levels of sensitivity against elevated ozone. Environ. Exp. Bot. 2018, 155, 66–78. [Google Scholar] [CrossRef]
  38. Semer, J.; Navrátil, M.; Špunda, V.; Štroch, M. Chlorophyll fluorescence parameters to assess utilization of excitation energy in photosystem II independently of changes in leaf absorption. J. Photochem. Photobiol. B Biol. 2019, 197, 1–11. [Google Scholar] [CrossRef]
  39. Pietrini, F.; Iori, V.; Beone, T.; Mirabile, D.; Zacchini, M. Effects of a ladle furnace slag added to soil on morpho-physiological and biochemical parameters of Amaranthus paniculatus L. plants. J. Hazard. Mater. 2017, 329, 339–347. [Google Scholar] [CrossRef] [PubMed]
  40. Dai, L.; Li, P.; Shang, B.; Liu, S.; Yang, A.; Wang, Y.; Feng, Z. Differential responses of peach (Prunus persica) seedlings to elevated ozone are related with leaf mass per area, antioxidant enzymes activity rather than stomatal conductance. Environ. Pollut. 2017, 227, 380–388. [Google Scholar] [CrossRef]
  41. Fu, W.; Liu, D.; Yin, Q.; Wu, Y.; Li, P. Suspended sediment in tidal currents: An often-neglected pollutant that aggravates mangrove degradation. Mar. Pollut. Bull. 2014, 84, 164–171. [Google Scholar] [CrossRef]
  42. Kaur, P.; Bali, S.; Sharma, A.; Vig, A.P.; Bhardwaj, R. Effect of earthworms on growth, photosynthetic efficiency and metal uptake in Brassica juncea L. plants grown in cadmium-polluted soils. Environ. Sci. Pollut. Res. 2017, 24, 13452–13465. [Google Scholar] [CrossRef] [PubMed]
  43. Kovács, H.; Aleksza, D.; Baba, A.I.; Hajdu, A.; Király, A.M.; Zsigmond, L.; Tóth, S.Z.; Kozma-Bognár, L.; Szabados, L. Light Control of Salt-Induced Proline Accumulation Is Mediated by ELONGATED HYPOCOTYL 5 in Arabidopsis. Front. Plant Sci. 2019, 10, 1–14. [Google Scholar] [CrossRef]
  44. Lin, K.H.; Huang, M.Y.; Huang, W.D.; Hsu, M.H.; Yang, Z.W.; Yang, C.M. The effects of red, blue, and white light-emitting diodes on the growth, development, and edible quality of hydroponically grown lettuce (Lactuca sativa L. var. capitata). Sci. Hortic. 2013, 150, 86–91. [Google Scholar] [CrossRef]
  45. Hogewoning, S.W.; Trouwborst, G.; Maljaars, H.; Poorter, H.; van Ieperen, W.; Harbinson, J. Blue light dose-responses of leaf photosynthesis, morphology, and chemical composition of Cucumis sativus grown under different combinations of red and blue light. J. Exp. Bot. 2010, 61, 3107–3117. [Google Scholar] [CrossRef]
  46. Dong, C.; Fu, Y.; Liu, G.; Liu, H. Growth, Photosynthetic Characteristics, Antioxidant Capacity and Biomass Yield and Quality of Wheat (Triticum aestivum L.) Exposed to LED Light Sources with Different Spectra Combinations. J. Agron. Crop Sci. 2014, 200, 219–230. [Google Scholar] [CrossRef]
  47. Luo, J.; He, W. Sensitivity of Eucalyptus globulus to red and blue light with different combinations and their influence on its efficacy for contaminated soil phytoremediation. J. Environ. Manag. 2019, 241, 1–33. [Google Scholar] [CrossRef] [PubMed]
  48. Wang, W.X.; Rainbow, P.S. Subcellular partitioning and the prediction of cadmium toxicity to aquatic organisms. Environ. Chem. 2006, 3, 395–399. [Google Scholar] [CrossRef]
  49. Kwon, H.K.; Jeon, J.Y.; Oh, S.J. Potential for heavy metal (copper and zinc) removal from contaminated marine sediments using microalgae and light emitting diodes. Ocean Sci. J. 2017, 52, 57–66. [Google Scholar] [CrossRef]
  50. Wan, X.M.; Lei, M.; Chen, T.B.; Yang, J.X.; Liu, H.T.; Chen, Y. Role of transpiration in arsenic accumulation of hyperaccumulator Pteris vittata L. Environ. Sci. Pollut. Res. 2015, 22, 16631–16639. [Google Scholar] [CrossRef]
  51. Žaltauskaite, J.; Sodiene, I. Effects of cadmium and lead on the life-cycle parameters of juvenile earthworm Eisenia fetida. Ecotoxicol. Environ. Saf. 2014, 103, 9–16. [Google Scholar] [CrossRef]
  52. Lin, R.; Wang, X.; Luo, Y.; Du, W.; Guo, H.; Yin, D. Effects of soil cadmium on growth, oxidative stress and antioxidant system in wheat seedlings (Triticum aestivum L.). Chemosphere 2007, 69, 89–98. [Google Scholar] [CrossRef] [PubMed]
  53. Khan, M.M.; Islam, E.; Irem, S.; Akhtar, K.; Ashraf, M.Y.; Iqbal, J.; Liu, D. Pb-induced phytotoxicity in para grass (Brachiaria mutica) and Castorbean (Ricinus communis L.): Antioxidant and ultrastructural studies. Chemosphere 2018, 200, 257–265. [Google Scholar] [CrossRef] [PubMed]
  54. Wu, M.; Luo, Q.; Liu, S.; Zhao, Y.; Long, Y.; Pan, Y. Screening ornamental plants to identify potential Cd hyperaccumulators for bioremediation. Ecotoxicol. Environ. Saf. 2018, 162, 35–41. [Google Scholar] [CrossRef] [PubMed]
  55. Blomster, T.; Salojärvi, J.; Sipari, N.; Brosché, M.; Ahlfors, R.; Keinänen, M.; Overmyer, K.; Kangasjärvi, J. Apoplastic reactive oxygen species transiently decrease auxin signaling and cause stress-induced morphogenic response in Arabidopsis. Plant Physiol. 2011, 157, 1866–1883. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  56. Li, Y.F.; Gao, L.M.; Han, R. He–Ne laser illumination ameliorates photochemical impairment in ultraviolet-B stressed-wheat seedlings via detoxifying ROS cytotoxicity. Russ. J. Plant Physiol. 2017, 64, 766–775. [Google Scholar] [CrossRef]
  57. Konishi, N.; Ishiyama, K.; Matsuoka, K.; Maru, I.; Hayakawa, T.; Yamaya, T.; Kojima, S. NADH-dependent glutamate synthase plays a crucial role in assimilating ammonium in the Arabidopsis root. Physiol. Plant. 2014, 152, 138–151. [Google Scholar] [CrossRef] [PubMed]
  58. Kumar, N.; Krishnani, K.K.; Singh, N.P. Oxidative and cellular stress as bioindicators for metal contamination in freshwater mollusk Lamellidens marginalis. Environ. Sci. Pollut. Res. 2017, 24, 16137–16147. [Google Scholar] [CrossRef] [PubMed]
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Figure 1. Dry weight of A. thaliana under different light treatments.
Figure 1. Dry weight of A. thaliana under different light treatments.
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Figure 2. Content of Cd in A. thaliana roots and shoots under different treatments.
Figure 2. Content of Cd in A. thaliana roots and shoots under different treatments.
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Figure 3. Levels of H2O2 and MDA in A. thaliana shoots under different treatments.
Figure 3. Levels of H2O2 and MDA in A. thaliana shoots under different treatments.
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Figure 4. Chlorophyll fluorescence parameters of A. thaliana under different treatments.
Figure 4. Chlorophyll fluorescence parameters of A. thaliana under different treatments.
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Table
Table 1. Levels of amino acids (µmol kg−1 FW) in A. thaliana under different treatments.
Table 1. Levels of amino acids (µmol kg−1 FW) in A. thaliana under different treatments.
GluGlnAspAsnPro
CK973 ± 11 a2331 ± 161 b1012 ± 89 cd3129 ± 73 c363 ± 12 d
B0981 ± 31 a2591 ± 87 a1087 ± 76 c3256 ± 161 bc337 ± 13 e
B10902 ± 20 b2234 ± 107 b1352 ± 119 ab3579 ± 113 a387 ± 11 c
B50863 ± 19 c1981 ± 126 c1434 ± 56 a3432 ± 95 ab412 ± 9 b
B75817 ± 17 d1862 ± 89 c1223 ± 89 bc3316 ± 63 b391 ± 7 c
B100726 ± 29 e1573 ± 102 d932 ± 51 d2671 ± 89 d439 ± 13 a
Different letters mean significant differences in amino acid concentrations in A. thaliana shoots (p < 0.05) judged by Fisher’s LSD post-hoc tests.
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Chen, Y.; Liang, L.; Chen, D.; Gan, T.; Cao, M.; Luo, J. Alterations of Amino Acid Concentrations and Photosynthetic Indices in Light Irradiated Arabidopsis thaliana during Phytoextraction. Sustainability 2021, 13, 7720. https://doi.org/10.3390/su13147720

AMA Style

Chen Y, Liang L, Chen D, Gan T, Cao M, Luo J. Alterations of Amino Acid Concentrations and Photosynthetic Indices in Light Irradiated Arabidopsis thaliana during Phytoextraction. Sustainability. 2021; 13(14):7720. https://doi.org/10.3390/su13147720

Chicago/Turabian Style

Chen, Yanmei, Longfei Liang, Dan Chen, Tian Gan, Min Cao, and Jie Luo. 2021. "Alterations of Amino Acid Concentrations and Photosynthetic Indices in Light Irradiated Arabidopsis thaliana during Phytoextraction" Sustainability 13, no. 14: 7720. https://doi.org/10.3390/su13147720

APA Style

Chen, Y., Liang, L., Chen, D., Gan, T., Cao, M., & Luo, J. (2021). Alterations of Amino Acid Concentrations and Photosynthetic Indices in Light Irradiated Arabidopsis thaliana during Phytoextraction. Sustainability, 13(14), 7720. https://doi.org/10.3390/su13147720

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