Next Article in Journal
Bioactive Compounds in Moringa oleifera: Mechanisms of Action, Focus on Their Anti-Inflammatory Properties
Next Article in Special Issue
Mixing Compost and Biochar Can Enhance the Chemical and Biological Recovery of Soils Contaminated by Potentially Toxic Elements
Previous Article in Journal
Health and Environmental Hazards of the Toxic Pteridium aquilinum (L.) Kuhn (Bracken Fern)
Previous Article in Special Issue
In Vitro Culture Studies for the Mitigation of Heavy Metal Stress in Plants
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Plants
Volume 13
Issue 1
10.3390/plants13010019
plants-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Ameliorating Effects of Graphene Oxide on Cadmium Accumulation and Eco-Physiological Characteristics in a Greening Hyperaccumulator (Lonicera japonica Thunb.)

by
Zhouli Liu
1,2,3,4,*,
Qingxuan Lu
1,2,3,4,
Yi Zhao
5,*,
Jianbing Wei
1,2,3,4,
Miao Liu
6,
Xiangbo Duan
1,2,3,4 and
Maosen Lin
7
1
College of Life Science and Engineering, Shenyang University, Shenyang 110044, China
2
Institute of Carbon Neutrality Technology and Policy, Shenyang University, Shenyang 110044, China
3
Northeast Geological S&T Innovation Center of China Geological Survey, Shenyang 110000, China
4
Key Laboratory of Black Soil Evolution and Ecological Effect, Ministry of Natural Resources, Shenyang 110000, China
5
School of Chemistry and Environmental Engineering, Liaoning University of Technology, Jinzhou 121001, China
6
Institute of Applied Ecology, Chinese Academy of Sciences, Shenyang 110016, China
7
College of Water Conservancy, Shenyang Agricultural University, Shenyang 110161, China
*
Authors to whom correspondence should be addressed.
Plants 2024, 13(1), 19; https://doi.org/10.3390/plants13010019
Submission received: 9 November 2023 / Revised: 25 November 2023 / Accepted: 27 November 2023 / Published: 20 December 2023
(This article belongs to the Special Issue Phytomonitoring and Phytoremediation of Environmental Pollutants)
Browse Figures
Versions Notes

Abstract

:
Graphene oxide (GO), as a novel carbon-based nanomaterial (CBN), has been widely applied to every respect of social life due to its unique composite properties. The widespread use of GO inevitably promotes its interaction with heavy metal cadmium (Cd), and influences its functional behavior. However, little information is available on the effects of GO on greening hyperaccumulators under co-occurring Cd. In this study, we chose a typical greening hyperaccumulator (Lonicera japonica Thunb.) to show the effect of GO on Cd accumulation, growth, net photosynthesis rate (Pn), carbon sequestration and oxygen release functions of the plant under Cd stress. The different GO-Cd treatments were set up by (0, 10, 50 and 100 mg L−1) GO and (0, 5 and 25 mg L−1) Cd in solution culture. The maximum rate of Cd accumulation in the roots and shoots of the plant were increased by 10 mg L−1 GO (exposed to 5 mg L−1 Cd), indicating that low-concentration GO (10 mg L−1) combined with low-concentration Cd (5 mg L−1) might stimulate the absorption of Cd by L. japonica. Under GO treatments without Cd, the dry weight of root and shoot biomass, Pn value, carbon sequestration per unit leaf area and oxygen release per unit leaf area all increased in various degrees, especially under 10 mg L−1 GO, were 20.67%, 12.04%, 35% and 28.73% higher than the control. Under GO-Cd treatments, it is observed that the cooperation of low-concentration GO (10 mg L−1) and low-concentration Cd (5 mg L−1) could significantly stimulate Cd accumulation, growth, photosynthesis, carbon sequestration and oxygen release functions of the plant. These results indicated that suitable concentrations of GO could significantly alleviate the effects of Cd on L. japonica, which is helpful for expanding the phytoremediation application of greening hyperaccumulators faced with coexistence with environment of nanomaterials and heavy metals.

1. Introduction

Nanomaterials (NMs) with a series of superior performances have been widely used in medicine, mechanics, electronics, agriculture and the energy field [1,2,3,4]. As one of the most attractive NMs with multiple forms, carbon-based nanomaterials (CBNs) with nano-sized and unique physico-chemical properties, including graphene oxide (GO), single-walled carbon nanotubes, multiple-walled carbon nanotubes, carbon nanoparticles and fullerenes, provoke tremendous scientific interest for nanotechnology development of a wide range of medical and industrial applications [5,6,7,8,9,10,11,12,13,14]. Among them, GO, as a novel CBN, presents the widest application duo to more fascinating properties, such as high surface area, good thermal stability, excellent mechanical strength, high optical transmittance and electrical conductivity [15,16,17,18]. As a chemically modified graphene, GO contains a single-atom-thick two-dimensional sheet of carbon atoms [19,20]. GO carries large numbers of oxygen-containing functional groups such as alcohols, epoxides and carboxylic acids, and thus has exceptional structure characteristics, in which numerous hydrophobic sp(2) clusters are isolated within the hydrophilic sp(3) C-O matrix [21,22,23]. Because of those unique composite properties, GO has been widely applied to every respect of social life especially in the biomedical field such as drug delivery, biosensors, antibiotics, vaccine enhancers, photo-thermal therapy and cancer treatments [24,25,26,27,28,29]. By 2020, the market for GO products is approaching $675 million, which may result in a large number of graphene-based waste [30]. The intense demand and broad application of GO will lead to a significant increase in the amount of GO released into the environment, which may further bring unpredictable effects on human health, organism and ecology security [31]. Therefore, it is a critical issue for clarifying the potential effect of GO on organism.
Currently, numerous reports have documented the effects of GO on bacteria, animals and humans [32,33,34,35,36,37], and a few studies concern the effect of GO on crop plants. For instance, Begum et al. [38] reported that, under hydroponic conditions, a large number of GO accumulated on the roots of cabbage, tomato and red spinach which eventually resulted in the growth inhibition of these plants. A similar phenomenon was also found by Jiao et al. [39], which showed that GO in solution culture could significantly cause stress damage of plant cells and decrease the length of tobacco roots. Cheng et al. [40] showed that GO could lead to a decrease in the fresh root weight in Brassica napus L. In contrast, Hu et al. [41] reported that 0.1–10 mg L−1 GO did not significantly inhibit the root and shoot length of wheat (Triticum aestivum L.) compared with the control. He et al. [23] found that GO could stimulate the growth of plant, and low-concentration GO significantly promoted the germination of spinach and chive. Gao et al. [42] investigated that low-concentration GO exhibited a limited toxic effect on wheat and 5–40 mg L−1 GO stimulated a significant increase in the Cd content in the plant. A previous study showed that 5 mg L−1 GO had a promoting effect on the fresh weight of root and overground part of rice seedlings and 50 mg L−1 GO had an inhibitive effect on the fresh weight of the overground part of the plant [43]. Jiao et al. [44] observed that 20 mg L−1 GO promoted tomato root growth. Guo et al. [45] also showed that 50 and 100 mg L−1 GO enhanced the root development and increased biomass accumulation of mature tomato plants, and 200 mg L−1 GO did not significantly affect plant growth. This difference above may be related to plant species, GO concentrations and exposure duration [46]. However, these results above were based on limited research and lack of better knowledge about more plant species. Greening plants are important living components of the urban ecosystem, while few studies on GO involved greening plants; therefore, it was very necessary to assess the effect of different concentrations of GO on the greening plants.
In urban environments, pollutants cannot exist in isolation. In addition to the potential impact of GO, excessive heavy metals derived from the metallurgy and mining industry, exhaust emission and sewage irrigation were released into the urban environment and pose a serious threat to the survival of human beings and greening plants [47,48,49,50,51]. Cadmium (Cd), as one of the most toxic heavy metals, has become a global issue of common concern due to its high persistency, strong water solubility and carcinogenicity [52,53,54]. The content of Cd in soil exceeds the safety standard of the national soil quality, which will not only result in the inhibition of the eco-physiological characteristics including plant growth, photosynthesis and carbon sequestration and oxygen release functions, but also bring threats to human health induced by food chain transmission [55,56,57,58]. In this case, it is an urgent necessity to resolve the Cd contamination in the urban environment. Phytoremediation is an emerging technology of contamination control, which takes advantage of a hyperaccumulator to clean up hazardous heavy metals in environment [59,60,61]. Meanwhile, GO is considered as an efficient adsorbent CBNs applied to remove heavy metals from aquatic environment or wastewater due to its excellent physicochemical properties, such as strong hydrophilia, abundant oxygen functional groups, and large specific surface area [9,11,12,20,30,62,63,64,65]. It is obvious to show that greening hyperaccumulator and GO are both beneficial for removing heavy metals in contaminated urban environment; however, little information is available on the effects of GO on a greening hyperaccumulator under heavy-metal Cd stress.
Lonicera japonica Thunb. is a popular greening plant in urban areas and has various excellent characteristics such as easy cultivation, high biomass and strong resistance [66]. Our previous studies reported that L. japonica can accumulate cadmium (Cd) in stems and shoots above 100 μg g−1 dry tissue [67], which is the threshold value of a Cd-hyperaccumulator, and it is considered as a new woody Cd-hyperaccumulator [68,69,70,71,72,73,74]. In the present study, L. japonica, as a typical greening hyperaccumulator, is chosen to clarify the effect of GO on Cd accumulation and eco-physiological characteristics (including the growth, photosynthetic parameters, carbon sequestration and oxygen release functions) of the plant under Cd stress. It will be helpful to acquire a better understanding with the eco-physiological mechanisms of greening plants faced with an environment of nanomaterials and heavy metals, and confirm the phytoremediation potential of a woody greening hyperaccumulator regulated by a novel CBNs (GO).

2. Materials and Methods

2.1. Chemicals

The GO used in the study is a GO aqueous dispersion (5 mg mL−1, single-layer GO content > 98%, particle size 0.5–5 μm) purchased from Jiangsu Xianfeng Nano Material Technology Co., Ltd. (Nanjing, China), which has the characteristics of good water solubility, low impurities and strong stability. It was prepared using the improved Hummers method, and then subjected to ultrasonic treatment in deionized water to obtain a stable GO aqueous dispersion. CdCl2·2.5H2O (analytically pure, >99%) and all other chemicals were obtained from Kermel Chemical Reagent Co., Ltd. (Tianjin, China).

2.2. Materials and Treatments

Plant materials (Lonicera japonica Thunb.) in the study were derived from a non-contaminated field of Shenyang Agricultural University and propagated in sterilized sand. After 8 weeks, uniform plants were transformed to 500 mL adumbral containers with nutrient medium, 4 plants for each container, placed in an artificial climate chamber under controlled conditions: 16 h light/8 h dark cycle, 800–1000 μmol m−2 s−1 photosynthetic photo flux density (PPFD), with a 25 °C/18 °C day/night temperature and a relative humidity of 60%. The nutrient medium was the modified Hoagland solution containing the following ingredients (mmol L−1): Ca(NO3)2 × 4H2O 5.00, MgSO4 × 7H2O 2.00, KNO3 5.00, KH2PO4 1.00, H3BO3 0.05, ZnSO4 × 7H2O 0.80 × 10−3, MnCl2 × 4H2O 9.00 × 10−3, CuSO4 × 5H2O 0.30 × 10−3, (NH4)6Mo7O24 × 4H2O 0.02 × 10−3, Fe-EDTA 0.10. The pH of each solution was adjusted daily to 5.8 ± 0.1 with 0.1 M HCl or 0.1 M NaOH, and the nutrient medium in each container was renewed once every 3 days. Different concentrations of Cd2+ (0, 5 and 25 mg L−1) were obtained by CdCl2·2.5H2O solution. According to the reported ranges of concentrations in previous studies [49,50,51], the experiment sets up four GO treatments, which contain 0, 10, 50 and 100 mg L−1, respectively. The combined concentrations of GO and Cd (GO-Cd) were prepared by mixing GO and Cd alone, and twelve GO-Cd treatments were set up in the study as follows in Table 1. Four replications were applied in each GO-Cd treatment experiment. The seedlings of L. japonica were collected for analysis 4 weeks after GO-Cd treatment initiation.

2.3. Determination of Plant Biomass and Cd Content

The harvested plants were rinsed with tap water, and then separated into root and shoots. These plant tissues were separately rinsed with distilled water and finally with deionized water, wiped for surface moisture and weighed. These plant tissues were dried at 105 °C for 20 min, then they were dried at 70 °C until the weight became constant [72].
Dried plant tissues were weighed and ground to fine powder. These fine powders were digested with a concentrated acid mixture of HNO3/HClO4 (3:1, v/v) in a microwave digestion instrument (MARS5, CEM, Matthews, NC, USA). The Cd contents in the plant tissues (root and shoots) were determined by a flame atomic absorption spectrometer (AAS 3110 Perkin-Elmer, Waltham, MA, USA).

2.4. Assays of Photosynthetic Parameters

As one of the most important photosynthetic parameters, the net photosynthetic rate (Pn) of the plant was measured by a portable LI-6400 photosynthesis system (Lincoln, NE, USA) under different GO-Cd treatments. During the process of GO-Cd treatments, these parameters including light level, CO2 concentration and leaf temperature inside the leaf chamber were kept stable at 1000 μmol m−2 s−1 PPFD, 25 ± 0.3 °C and 380 ± 5 μmol CO2 mol−1.

2.5. Analysis of Carbon Sequestration and Oxygen Release Functions

The functions of carbon sequestration and oxygen release were measured according to the previous research [75]. The values of carbon sequestration and oxygen release values were decided by diurnal assimilation amounts (P) that can be calculated as Equation (1):
P = ∑ i = 1 j [ ( p i + 1 + p i ) ÷ 2 × ( t i + 1 − t i ) × 3600 ÷ 1000 ]
where P is the diurnal assimilation amount (mmol m−2 s−1), pi is the instantaneous photosynthetic rate at the initial measurement point (μmol m−2 s−1), pi+1 is the instantaneous photosynthetic rate of the next measurement point (μmol m−2 s−1), ti is the instantaneous time of the initial measurement point (h), ti+1 is the instantaneous time of the next measurement point (h), j is test times, 3600 refers to 3600 s per hour, and 1000 refers to 1000 μmol per mmol.
Carbon sequestration per unit leaf area (WCO2) and oxygen release per unit leaf area (WO2) of the plant can be calculated as Equations (2) and (3):
WCO2 = P × 44/1000
WO2 = P × 32/1000
where WCO2 is carbon sequestration per unit leaf area (g m−2 d−1), 44 is the molar mass of CO2; WO2 is oxygen release per unit leaf area (g m−2 d−1), 32 is the molar mass of O2.

2.6. Statistical Analyses

The data in the study are presented as means ± SD (standard deviation). SPSS 22.0 (SPSS Inc., Chicago, IL, USA) and Microsoft Office Excel 2020 (Microsoft Corporation, Redmond, WA, USA) were applied for statistical analysis. The significant differences between the GO-Cd treatments were presented at the p < 0.01 and p < 0.05 levels.

3. Results and Discussion

3.1. Cd Accumulation of L. japonica

After 4-week GO-Cd treatments, Cd contents in root and shoots of L. japonica are shown in Figure 1. With the increase in Cd concentration in solution, Cd contents in roots and shoots of L. japonica all increased significantly compared to the control, which is consistent with our previous research findings [69,70,74]. Under 5 and 25 mg L−1 Cd stress without GO treatments, the Cd contents in the root of the plant were 223.75 ± 17.23 μg g−1 (GO0-Cd5) and 800.25 ± 31.84 μg g−1 DW (GO0-Cd25). Under GO treatments, the Cd contents in the root of the plant had an increasing trend compared with the control, especially exposed to high concentrations (10 and 50 mg L−1) GO in solution. Under 5 and 25 mg L−1 Cd stress, the Cd contents in the root of the plant were enhanced significantly by 10 mg L−1 GO treatment (p < 0.01), which reached 318.13 ± 22.05 μg g−1 DW (GO10-Cd5) and 949.67 ± 52.14 μg g−1 DW (GO10-Cd25), respectively. Similar results were reported by Yin et al. [76], who found that 100 to 500 mg L−1 GO promoted the increased Cd contents in roots of maize exposed to 20 mg L−1 Cd, possibly due to Cd2+ in roots more adsorbed through adhering GO particles. When the GO concentration in solution was added to 50 mg L−1 (exposed to 5 and 25 mg L−1 Cd), the Cd contents in the root of the plant increased significantly (p < 0.05), which reached 257.38 ± 18.10 μg g−1 DW (GO50-Cd5) and 903.41 ± 32.29 μg g−1 DW (GO50-Cd25), raising by 15.03% and 12.89% compared with the GO0-Cd5 and GO0-Cd25 treatments. Our research results are in agreement with the results of the study by Gao et al. [42], who showed that when GO was supplied to wheat in root tissues, low-concentration GO promoted a significant increase in Cd content in wheat. With the increase in GO concentration in solution, the Cd contents in root of the plant had no significant increase compared with the GO0-Cd5 (T2) and GO0-Cd25 (T3) treatments. The reason might be that the limited root surface area cause the root to not be able to adhere more GO particles, or that the carboxylate groups at GO edges provide active sites to accumulate Cd2+ in the interlayer space and reduce root uptake gradually [76,77].
By comparison, the Cd contents in shoots of L. japonica had a similar change trend with the Cd contents in root under different GO-Cd treatments. Under 5 and 25 mg L−1 Cd stress, the Cd contents in shoots of the plant were enhanced significantly by 10 mg/L GO treatment (p < 0.01), which reached 63.42 ± 8.55 μg g−1 DW (GO10-Cd5) and 320.03.67 ± 9.47 μg g−1 DW (GO10-Cd25), respectively. When the GO concentration in solution was added to 50 mg L−1 (exposed to 5 and 25 mg L−1 Cd), the Cd contents in shoots of the plant had an increased trend, which reached 58.36 ± 5.94 μg g−1 DW (GO50-Cd5) and 311.29 ± 13.51 μg g−1 DW (GO50-Cd25), raising by 23.96% and 6.21% compared with the GO0-Cd5 and GO0-Cd25 treatments. With the increase in GO concentration in solution, the Cd contents in shoots of the plant had no significant increase compared with the GO0-Cd5 (T2) and GO0-Cd25 (T3) treatments. This is may be due to the reason that GO can directly and indirectly regulate the uptake of heavy metals and the regulation effect was concentration-dependent [41]. The maximum rates of Cd accumulation in roots and shoots of the plant increased by 10 mg L−1 GO (exposed to 5 mg L−1 Cd) were 42.18% and 34.71% compared with the GO0-Cd5 (T2) treatment, indicating that low-concentration GO (10 mg L−1) combined with low-concentration Cd (5 mg L−1) might stimulate the absorption of Cd by L. japonica, which could be applied on a suitable concentration GO-enhanced phytoremediation of L. japonica under a Cd-contaminated environment. The suitable GO concentration is important for improving phytoremediation ability. This is possibly because suitable concentration GO can positively modulate the metabolic processes and adsorption mechanisms in L. japonica including the improved eco-physiological responses for maintaining good tolerance, the stimulated activity of antioxidant enzymes to reduce excessive reactive oxygen species (ROS) production, and the promoted conversion of exchangeable Cd2+ which is more available for plant absorption. The specific mechanism still needs further exploration. Positive effects of GO on Cd accumulation in duckweed were also observed by Yang et al. [78]. The possible reasons for this are the large specific surface area and adsorption capacity of GO, co-transport of GO and heavy metal, and regulated transporter gene expression [79,80,81].

3.2. Growth Charateristics of L. japonica

Several studies found that growth indicators are a sensitive parameter when the plants are subject to external environmental stress [82,83]. After 4-week GO-Cd treatments, the growth characteristics in terms of root and shoot biomass dry weight in L. japonica are shown in Figure 2. Under T1–T3 treatments (under Cd stress without GO treatments), the dry weight of root biomass increased significantly exposed to 5 mg L−1 Cd (p < 0.05), then had a decreased trend exposed to 25 mg L−1 Cd and had no significant change compared with the control, indicating that low-concentration Cd could promote the growth of the plant. The results are in accordance with our previous studies, which observed an inverted U-shaped dose–response curve of the growth characteristics under different concentrations of Cd treatments, indicating that the hormetic effect of low-concentration Cd occurred in L. japonica [68,69,70,71,72,84]. The phenomenon of hormesis has also been found in barley [85]. Under GO treatments without Cd stress (T4, T7 and T10), the dry weight of root biomass showed an increase, especially under 10 mg L−1 GO (T4), 20.67% higher than the control (T1, GO0-Cd0), which may due to the reason that the GO with various oxygen-containing functional groups collected water, and the hydrophobic sp(2) domains of GO transported water to the roots to accelerate the growth of plants [23]. Under GO treatments and Cd stress (T5, T6, T8, T9, T11 and T12), different concentrations of GO increased the dry weight of root biomass exposed to different concentrations of Cd, especially under 10 mg L−1 GO; the dry weight of root biomass exposed to 5 mg L−1 Cd (T5) and 25 mg L−1 Cd (T6) were enhanced significantly by 34.85% and 33.33% higher than the GO0-Cd5 (T2) and GO0-Cd25 (T3) treatments, which showed that the cooperation of low-concentration GO (10 mg L−1) and low-concentration Cd (5 mg L−1) could significantly promote the growth of root, and with the increase in Cd stress, 10 mg L−1 GO could alleviate the toxic effect of Cd on the root of the plant. A similar phenomenon was also observed by He et al. [77], who found that the seedlings of the rice (Oryza sativa L. ssp. japonica) showed the largest fresh weight value under Cd and GO treatments. The reason might be that low-concentration GO is relatively biocompatible [86,87] and could provide water and enhance nutrients for plant growth within limits [23,88]. Higher-concentration GO could affect the permeability of cell membranes and metabolic processes of plants [78].
In contrast to root, the dry weight of shoot biomass of L. japonica had a similar change trend under different GO-Cd treatments. Under T1–T3 treatments (under Cd stress without GO treatments), the dry weight of shoot biomass showed an inverted U-shaped dose–response curve, indicating that the low-concentration Cd had a hormetic effect on the growth of shoots. Under GO treatments without Cd stress (T4, T7 and T10), the dry weight of shoot biomass showed an increase, especially under 10 mg L−1 GO (T4), 12.04% higher than the control (T1, GO0-Cd0). A similar phenomenon was also reported by other researchers when the plants were subjected to different environmental stresses, which is considered as hormesis that may have resulted from the overcompensating behavior of the organism responding to the disrupted homeostasis [89,90,91,92,93,94]. Under GO treatments and Cd stress (T5, T6, T8, T9, T11 and T12), different concentrations of GO increased the dry weight of shoot biomass exposed to different concentrations of Cd, especially under 10 mg L−1 GO; the dry weight of shoots biomass exposed to 5 mg L−1 Cd (T5) were enhanced significantly and reached 4.69 ± 0.22 μg g−1 DW, increasing by 14.11% compared with the GO0-Cd5 (T2) treatment, which showed that low-concentration GO (10 mg L−1) combined with low-concentration Cd (5 mg L−1) could significantly stimulate the growth of shoots. With the increase in GO concentration in solution, the dry weight of root and shoot biomass had no significant increase compared with the T1–T3 treatments (under Cd stress without GO treatments), which indicated that GO has a limited concentration effect on alleviating the toxic effect of Cd, and the enhanced accumulation of Cd in roots and shoots stimulated by GO might gradually lead to the increase in cytotoxicity. The results are consistent with the findings of Hu et al. [41] and Yin et al. [76], who proposed that the effects of GO on plant growth depend on GO concentration.

3.3. Photosynthetic Parameters of L. japonica

Photosynthesis of plants is the source of the material and energy required by most organisms on earth; however, as a sensitive site for environmental factors, photosynthesis is susceptible to external environmental changes [95]. It is reported that the net photosynthesis rate (Pn) is usually used as an important indicator for measuring the ability of light energy utilization [96]. The effects of different GO-Cd treatments on Pn in L. japonica are shown in Figure 3. When the plant was exposed to 5 mg L−1 Cd stress without GO treatments (T2), the value of Pn in L. japonica increased significantly and reached 13.72 ± 0.51 μmol m−2 s−1, which is 20% compared with the control. With the increase in Cd stress, the value of Pn in L. japonica had a decreased trend and had no significant increase compared with the control, indicating that low-concentration Cd could stimulate the photosynthesis of the plant. The results are in agreement with the growth responses of L. japonica, which showed an inverted U-shaped dose–response curve under different concentrations of Cd treatments. Yet, several researchers found that different plants exhibit different response characteristics under GO treatments. Chen et al. [97] reported that GO had serious toxicity and induced the inhibition of photosynthesis in naked oats (Avena sativa L.). Zhao et al. [98] showed that GO exposure had adverse effects on the photosynthetic parameters of white clover (Trifolium repens L.), the reason for which may be a decreased metabolism, as shown by electron transport system activity [99]. Hazeem et al. [100] found that low concentrations of GO exposure can improve photosynthetic pigment content of the marine alga Picochlorum sp., and higher concentrations of GO exposure had a negative effect on the photosynthetic pigment content of the plant. However, in the present study, under GO treatments without Cd stress (T4, T7 and T10), the value of Pn in L. japonica showed an increasing trend, especially under 10 mg L−1 GO (T4), the value of Pn in the plant increased significantly, 35% higher than the control (T1, GO0-Cd0). The Pn value in L. japonica had an increase of 19% compared with the control when the plant was exposed to 50 mg L−1 GO (T7) treatment. The significant increase in Pn when L. japonica was exposed to low concentrations of GO treatments may stem from a stimulating effect by hormesis. A similar result was also found by Zhou et al. [101], which showed that GO exposure can promote photosynthesis performance of Iris pseudacorus. The reasons for this might result from optimizing the electron transport at the acceptor side of PSII and improving the energy conversion efficiency of PSII. When GO concentration in solution was up to 100 mg L−1, the value of Pn in L. japonica showed a slight increase of 6% and had no significant increase compared with the control, indicating that the plant still kept a good ability of light energy utilization even under high concentrations of GO treatment. Under GO treatments and Cd stress (T5, T6, T8, T9, T11 and T12), different concentrations of GO increased the value of Pn in L. japonica exposed to different concentrations Cd, especially under 10 mg L−1 GO, where the Pn value in L. japonica exposed to 5 mg L−1 Cd (T5) was enhanced significantly and reached 19.86 ± 0.42 μg g−1 DW, increasing by 45% compared with the GO0-Cd5 (T2) treatment, which showed that the cooperation of low-concentration GO (10 mg L−1) and low-concentration Cd (5 mg L−1) has dual hormetic effect on the photosynthesis of the plant. With the increase in GO and Cd concentrations in solution, the Pn value in L. japonica still kept an increase, indicating the plant did not suffer GO or metal toxicity and generated a product of metabolism for metal absorption, plant growth and photosynthesis, which might be related with the strong tolerance and hyperaccumulation characteristics of L. japonica combined with environmental stress [70,102].

3.4. Carbon Sequestration and Oxygen Release Functions of L. japonica

It is well known that carbon sequestration and oxygen release functions are considered as crucial parameters to assess the ability of plant photosynthesis [103]. To investigate carbon sequestration and oxygen release functions, it is helpful to explore the ecological service function of the greening plants [104]. The effect of different GO-Cd treatments on the carbon sequestration and oxygen release characteristics of L. japonica are shown in Table 2. In the present study, when L. japonica was exposed to 5 mg L−1 Cd stress without GO treatments (T2), the carbon sequestration per unit leaf area and oxygen release per unit leaf area of the plant had significant increases and reached 12.06 ± 0.31 g m−2 d−1, 8.77 ± 0.28 g m−2 d−1, respectively, which is 19.05% compared with the control. The results indicated that low-concentration Cd could stimulate the carbon sequestration and oxygen release functions of the plant, which is in agreement with the response of photosynthetic parameters in terms of increased Pn value. When Cd treatment concentration was up to 25 mg L−1, the carbon sequestration per unit leaf area and oxygen release per unit leaf area of L. japonica showed a slight increase of 11.35% and had no significant increase compared with the control. Under GO treatments without Cd stress (T4, T7 and T10), the carbon sequestration per unit leaf area and oxygen release per unit leaf area of L. japonica showed an increase, especially under 10 mg L−1 GO (T4), 28.73% higher than the control (T1, GO0-Cd0). When L. japonica was exposed to 10 mg L−1 GO treatment, the carbon sequestration per unit leaf area and oxygen release per unit leaf area of the plant had significant increases and reached 13.04 ± 0.53 g m−2 d−1 and 9.48 ± 0.21 g m−2 d−1, respectively. Under low concentrations of GO treatments, the significant increase in carbon sequestration and oxygen release values of L. japonica may result from the stimulated photosynthesis by hormesis effect, which is represented by the change in PN value. This is identical to the relevant study, which showed that main biological components required for carbon sequestration and oxygen release all source from the process of plant photosynthesis [105]. It was also reported that the greening plants with functional carbon sequestration and oxygen release characteristics could exchange more CO2 and O2 with the environmental medium, then change more light energy into nutrients stored in plants [106]. When GO treatment concentration was up to 100 mg L−1, the carbon sequestration per unit leaf area and oxygen release per unit leaf area of the plant had significant increases and reached 11.25 ± 0.29 g m−2 d−1 and 8.18 ± 0.36 g m−2 d−1, respectively, which is 11.06% compared with the control, indicating that the plant still had good functions of carbon sequestration and oxygen release even under high concentrations of GO treatment. Under GO treatments and Cd stress (T5, T6, T8, T9, T11 and T12), different concentrations of GO increased the carbon sequestration per unit leaf area and oxygen release per unit leaf area of the plant exposed to different concentrations of Cd, especially under 10 mg L−1 GO, where the carbon sequestration per unit leaf area and oxygen release per unit leaf area of the plant exposed to 5 mg L−1 Cd (T5) were enhanced significantly by 38.89% higher than the GO0-Cd5 (T2) treatment, which showed that the cooperation of low-concentration GO (10 mg L−1) and low-concentration Cd (5 mg L−1) could significantly stimulate the carbon sequestration and oxygen release functions of the plant (p < 0.01). It is shown that the carbon sequestration per unit leaf area could predict the carbon sequestration capacity of plants through their photosynthesis, and therefore it was directly used for the evaluation of the carbon sequestration functions in different types of plants [103,107]. In the present study, L. japonica still kept an increase by 20.34% compared to the control even under 100 mg L−1 GO and 25 mg L−1 Cd (T12) treatments, which indicated that the plant had a strong capacity of carbon sequestration under the mutual influence of environmental stress.

4. Conclusions

In the present study, the effect of GO on Cd accumulation and eco-physiological characteristics (including the growth, photosynthetic parameters, carbon sequestration and oxygen release functions) of L. japonica under different concentrations of Cd treatments were investigated. It is observed that the suitable GO concentration is important for improving phytoremediation ability. Low-concentration GO (10 mg L−1) combined with low-concentration Cd (5 mg L−1) might stimulate the absorption of Cd by L. japonica, which could be applied on a suitable concentration GO-enhanced phytoremediation of L. japonica under a Cd-contaminated environment. Under GO-Cd treatments, it is shown that the cooperation of low-concentration GO (10 mg L−1) and low-concentration Cd (5 mg L−1) could significantly stimulate the growth, photosynthesis, carbon sequestration and oxygen release functions of the plant. With the increase in treatment concentrations, L. japonica still kept an increase of 20.34% compared to the control even under 100 mg L−1 GO and 25 mg L−1 Cd treatments, which indicated that the plant had a strong capacity for carbon sequestration under the mutual influence of environmental stress. In our previous studies, it was investigated that L. japonica is a greening Cd-hyperaccumulator with dual merits of phytoremediation and decoration, which will bring social and environmental benefits on urban construction. Therefore, we will consider these good capacities of carbon sequestration and hyperaccumulation comprehensively by combing practical applications, which could provide a more reasonable suggestion for city’s policymakers. Otherwise, the study will supply referable achievement for the ecological responses of the greening plants to combined environmental stress.

Author Contributions

Conceptualization, Z.L., Q.L. and Y.Z; data curation, Z.L. and Y.Z.; formal analysis, Z.L. and X.D.; funding acquisition, Q.L.; methodology, Z.L. and J.W.; software, Z.L. and M.L. (Maosen Lin); writing—original draft, Z.L. and M.L. (Miao Liu); writing—review and editing, Z.L. and Q.L. All authors have read and agreed to the published version of the manuscript.

Funding

This study is financially supported by LiaoNing Revitalization Talents Program (XLYC2203070), the funding project of Northeast Geological S&T Innovation Center of China Geological Survey (QCJJ2022-44), the National Natural Science Foundation of China (41771200, 41171399, 32071580), the Young Scientists Fund of the National Natural Science Foundation of China (32201730, 42307433, 41301340, 41807172), Shenyang Science and Technology Bureau (22-322-3-14), the Innovation and Entrepreneurship Training Program for College Students (S202311035080), the Graduate Education and Teaching Reform Project of Shenyang University.

Data Availability Statement

Data are contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Su, S.; Kang, P.M. Systemic review of biodegradable nanomaterials in nanomedicine. Nanomaterials 2020, 10, 656. [Google Scholar] [CrossRef] [PubMed]
  2. Tripathi, A.; Bonilla-Cruz, J. Review on healthcare biosensing nanomaterials. ACS Appl. Nano Mater. 2023, 6, 5042–5074. [Google Scholar] [CrossRef]
  3. Costanzo, H.; Gooch, J.; Frascione, N. Nanomaterials for optical biosensors in forensic analysis. Talanta 2023, 253, 123945. [Google Scholar] [CrossRef] [PubMed]
  4. Zhang, Y.H.; Poon, K.; Masonsong, G.S.P.; Ramaswamy, Y.; Singh, G. Sustainable nanomaterials for biomedical applications. Pharmaceutics 2023, 15, 922. [Google Scholar] [CrossRef] [PubMed]
  5. Wan, S.; Bi, H.C.; Sun, L.T. Graphene and carbon-based nanomaterials as highly efficient adsorbents for oils and organic solvents. Nanotechnol. Rev. 2016, 5, 3–22. [Google Scholar] [CrossRef]
  6. Xin, Q.; Shah, H.; Nawaz, A.; Xie, W.J.; Akram, M.Z.; Batool, A.; Tian, L.Q.; Jan, S.U.; Boddula, R.; Guo, B.D.; et al. Antibacterial carbon-based nanomaterials. Adv. Mater. 2019, 31, 1804838. [Google Scholar] [CrossRef] [PubMed]
  7. Verma, S.K.; Das, A.K.; Gantait, S.; Panwar, Y.; Kumar, V.; Brestic, M. Green synthesis of carbon-based nanomaterials and their applications in various sectors: A topical review. Carbon. Lett. 2021, 32, 365–393. [Google Scholar] [CrossRef]
  8. Liu, H.Y.; Chen, J.L.; Qiao, S.; Zhang, W. Carbon-based nanomaterials for bone and cartilage regeneration: A review. ACS Biomater. Sci. Eng. 2021, 7, 4718–4735. [Google Scholar] [CrossRef]
  9. Devi, M.K.; Yaashikaa, P.R.; Kumar, P.S.; Manikandan, S.; Oviyapriya, M.; Varshika, V.; Rangasamy, G. Recent advances in carbon-based nanomaterials for the treatment of toxic inorganic pollutants in wastewater. New J. Chem. 2023, 47, 7655–7667. [Google Scholar] [CrossRef]
  10. Caffo, M.; Curcio, A.; Rajiv, K.; Caruso, G.; Venza, M.; Germano, A. Potential role of carbon nanomaterials in the treatment of malignant brain gliomas. Cancers 2023, 15, 2575. [Google Scholar] [CrossRef]
  11. Elsaid, K.; Olabi, A.G.; Abdel-Wahab, A.; Elkamel, A.; Alami, A.H.; Inayat, A.; Chae, K.J.; Abdelkareem, M.A. Membrane processes for environmental remediation of nanomaterials: Potentials and challenges. Sci. Total Environ. 2023, 879, 162569. [Google Scholar] [CrossRef]
  12. Mohapatra, L.; Cheon, D.; Yoo, S.H. Carbon-based nanomaterials for catalytic wastewater treatment: A review. Molecules 2023, 28, 1805. [Google Scholar] [CrossRef] [PubMed]
  13. Joze-Majidi, H.; Zabihi, E.; Arab-Bafrani, Z.; Mir, S.M.; Reiter, R.J. Comparative radiosensitization efficiency assessment of graphene oxide and Ti3C2 MXene as 2D carbon-based nanoparticles against breast cancer cells: Characterization, toxicity and mechanisms. 2D Mater. 2023, 10, 025021. [Google Scholar] [CrossRef]
  14. Pawar, S.; Duadi, H.; Fixler, D. Recent advances in the spintronic application of carbon-based nanomaterials. Nanomaterials 2023, 13, 598. [Google Scholar] [CrossRef] [PubMed]
  15. Sinha, A.; Ranjan, P.; Ali, A.; Balakrishnan, J.; Thakur, A.D. Graphene oxide and its derivatives as potential Ovchinnikov ferromagnets. J. Phys.-Condens. Matter 2021, 33, 375801. [Google Scholar] [CrossRef]
  16. Itoo, A.M.; Vemula, S.L.; Gupta, M.T.; Giram, M.V.; Kumar, S.A.; Ghosh, B.; Biswas, S. Multifunctional graphene oxide nanoparticles for drug delivery in cancer. J. Control. Release 2022, 350, 26–59. [Google Scholar] [CrossRef] [PubMed]
  17. Wang, P.J.; Duan, F.L. Tribochemistry of graphene oxide/graphene confined between iron oxide substrates: Implications for graphene-based lubricants. ACS Appl. Nano Mater. 2022, 5, 12817–12825. [Google Scholar] [CrossRef]
  18. Fu, X.; Lin, J.J.; Liang, Z.H.; Yao, R.H.; Wu, W.J.; Fang, Z.Q.; Zou, W.X.; Wu, Z.Y.; Ning, H.L.; Peng, J.B. Graphene oxide as a promising nanofiller for polymer composite. Surf. Interfaces 2023, 37, 102747. [Google Scholar] [CrossRef]
  19. Costa, M.C.F.; Marangoni, V.S.; Ng, P.R.; Nguyen, H.T.L.; Carvalho, A.; Neto, A.H.C. Accelerated synthesis of graphene oxide from graphene. Nanomaterials 2021, 11, 551. [Google Scholar] [CrossRef]
  20. Jia, F.C.; Xiao, X.; Nashalian, A.; Shen, S.; Yang, L.; Han, Z.Y.; Qu, H.J.; Wang, T.M.; Ye, Z.; Zhu, Z.J.; et al. Advances in graphene oxide membranes for water treatment. Nano Res. 2022, 15, 6636–6654. [Google Scholar] [CrossRef]
  21. Asghari, M.; Saadatmandi, S.; Afsari, M. Graphene oxide and its derivatives for gas separation membranes. Chembioeng. Rev. 2021, 8, 490–516. [Google Scholar] [CrossRef]
  22. Pandit, S.; Seth, S.; Bapli, A.; Bhattacharjee, S.; Seth, D. Graphene oxide induced prototropism in different solvents: Enhancement of fluorescence induced by graphene oxide. J. Mol. Liq. 2023, 369, 120880. [Google Scholar] [CrossRef]
  23. He, Y.J.; Hu, R.R.; Zhong, Y.J.; Zhao, X.L.; Chen, Q.; Zhu, H.W. Graphene oxide as a water transporter promoting germination of plants in soil. Nano Res. 2018, 11, 1928–1937. [Google Scholar] [CrossRef]
  24. Bolibok, P.; Koter, S.; Kaczmarek-Kedziera, A.; Kowalczyk, P.; Lukomska, B.; Lukomska, O.; Boncel, S.; Wisniewski, M.; Kaneko, K.; Terzyk, A.P. Liquid phase adsorption induced nanosizing of graphene oxide. Carbon 2021, 183, 948–957. [Google Scholar] [CrossRef]
  25. Chen, Y.W.; Su, X.Y.; Esmail, D.; Buck, E.; Tran, S.D.; Szkopek, T.; Cerruti, M. Dual-templating strategy for the fabrication of graphene oxide, reduced graphene oxide and composite scaffolds with hierarchical architectures. Carbon 2022, 189, 186–198. [Google Scholar] [CrossRef]
  26. Keramat, A.; Kadkhoda, J.; Farahzadi, R.; Fathi, E.; Davaran, S. The potential of graphene oxide and reduced graphene oxide in diagnosis and treatment of cancer. Curr. Med. Chem. 2022, 29, 4529–4546. [Google Scholar] [CrossRef] [PubMed]
  27. Oliveira, A.M.L.; Machado, M.; Silva, G.A.; Bitoque, D.B.; Ferreira, J.T.; Pinto, L.A.; Ferreira, Q. Graphene oxide thin films with drug delivery function. Nanomaterials 2022, 12, 1149. [Google Scholar] [CrossRef]
  28. Sellathurai, A.J.; Mypati, S.; Kontopoulou, M.; Barz, D.P.J. High yields of graphene nanoplatelets by liquid phase exfoliation using graphene oxide as a stabilizer. Chem. Eng. J. 2023, 451, 138365. [Google Scholar] [CrossRef]
  29. Dabrowski, B.; Zuchowska, A.; Brzozka, Z. Graphene oxide internalization into mammalian cells-a review. Colloid Surf. B 2023, 221, 112998. [Google Scholar] [CrossRef]
  30. Ahmed, F.; Rodrigues, D.F. Investigation of acute effects of graphene oxide on wastewater microbial community: A case study. J. Hazard Mater. 2013, 256–257, 33–39. [Google Scholar] [CrossRef]
  31. Shen, S.S.; Liu, Y.F.; Wang, F.; Yao, G.X.; Xie, L.L.; Xu, B.B. Graphene oxide regulates root development and influences IAA concentration in rice. J. Plant Growth. Regul. 2019, 38, 241–248. [Google Scholar] [CrossRef]
  32. Akhavan, O.; Ghaderi, E.; Esfandiar, A. Wrapping bacteria by graphene nanosheets for isolation from environment, reactivation by sonication, and inactivation by nearinfrared irradiation. J. Phys. Chem. B 2011, 115, 6279–6288. [Google Scholar] [CrossRef] [PubMed]
  33. Liu, J.H.; Yang, S.T.; Wang, H.; Chang, Y.; Cao, A.; Liu, Y. Effect of size and dose on the biodistribution of graphene oxide in mice. Nanomedicine 2012, 7, 1801–1812. [Google Scholar] [CrossRef] [PubMed]
  34. Lu, C.J.; Jiang, X.F.; Junaid, M.; Ma, Y.B.; Jia, P.P.; Wang, H.B.; Pei, D.S. Graphene oxide nanosheets induce DNA damage and activate the base excision repair (BER) signaling pathway both in vitro and in vivo. Chemosphere 2017, 184, 795–805. [Google Scholar] [CrossRef] [PubMed]
  35. Mittal, S.; Kumar, V.; Dhiman, N.; Chauhan, L.K.S.; Pasricha, R.; Pandey, A.K. Physico-chemical properties based differential toxicity of graphene oxide/reduced graphene oxide in human lung cells mediated through oxidative stress. Sci. Rep. 2017, 7, 39548. [Google Scholar] [CrossRef] [PubMed]
  36. Radunovic, M.; De Colli, M.; De Marco, P.; Di Nisio, C.; Fontana, A.; Piattelli, A.; Cataldi, A.; Zara, S. Graphene oxide enrichment of collagen membranes improves DPSCs differentiation and controls inflammation occurrence. J. Biomed. Mater. Res. A 2017, 105, 2312–2320. [Google Scholar] [CrossRef]
  37. Tabish, T.A.; Pranjol, M.Z.I.; Hayat, H.; Rahat, A.A.M.; Abdullah, T.M.; Whatmore, J.L.; Zhang, S.W. In vitro toxic effects of reduced graphene oxide nanosheets on lung cancer cells. Nanotechnology 2017, 28, 504001. [Google Scholar] [CrossRef]
  38. Begum, P.; Ikhtiari, R.; Fugetsu, B. Graphene phytotoxicity in the seedling stage of cabbage, tomato, red spinach, and lettuce. Carbon 2011, 49, 3907–3919. [Google Scholar] [CrossRef]
  39. Jiao, J.; Yuan, C.; Wang, J.; Xia, Z.; Xie, L.; Chen, F.; Li, Z.; Xu, B. The role of graphene oxide on tobacco root growth and its preliminary mechanism. J. Nanosci. Nanotechnol. 2016, 16, 12449–12454. [Google Scholar] [CrossRef]
  40. Cheng, F.; Liu, Y.F.; Lu, G.Y.; Zhang, X.K.; Xie, L.L.; Yuan, C.F.; Xu, B.B. Graphene oxide modulates root growth of Brassica napus L. and regulates ABA and IAA concentration. J. Plant Physiol. 2016, 193, 57–63. [Google Scholar] [CrossRef]
  41. Hu, X.; Kang, J.; Lu, K.; Zhou, R.; Mu, L.; Zhou, Q. Graphene oxide amplifies the phytotoxicity of arsenic in wheat. Sci. Rep. 2014, 4, 6122. [Google Scholar] [CrossRef] [PubMed]
  42. Gao, M.L.; Yang, Y.J.; Song, Z.G. Effects of graphene oxide on cadmium uptake and photosynthesis performance in wheat seedlings. Ecotoxicol. Environ. Safe 2019, 173, 165–173. [Google Scholar] [CrossRef] [PubMed]
  43. Liu, S.; Wei, H.; Li, Z.; Li, S.; Yan, H.; He, Y.; Tian, Z. Effects of graphene on germination and seedling morphology in rice. J. Nanosci. Nanotechnol. 2015, 15, 2695–2701. [Google Scholar] [CrossRef] [PubMed]
  44. Jiao, J.; Cheng, F.; Zhang, X.; Xie, L.; Li, Z.; Yuan, C.; Xu, B.; Zhang, L. Preparation of graphene oxide and its mechanism in promoting tomato roots growth. J. Nanosci. Nanotechnol. 2016, 16, 4216–4223. [Google Scholar] [CrossRef]
  45. Guo, X.H.; Zhao, J.G.; Wang, R.M.; Zhang, H.C.; Xing, B.Y.; Naeen, M.; Yao, T.J.; Li, R.Q.; Xu, R.F.; Zhang, Z.F.; et al. Effects of graphene oxide on tomato growth in different stages. Plant Physiol. Biochem. 2021, 162, 447–456. [Google Scholar] [CrossRef] [PubMed]
  46. Yang, Y.; Zhang, R.; Zhang, X.; Chen, Z.; Wang, H.; Li, P.C.H. Effects of graphene oxide on plant growth: A review. Plants 2022, 11, 2826. [Google Scholar] [CrossRef]
  47. Feller, U.; Anders, I.; Wei, S. Distribution and redistribution of 109Cd and 65Zn in the heavy metal hyperaccumulator Solanum nigrum L.: Influence of cadmium and zinc concentrations in the root medium. Plants 2019, 8, 340. [Google Scholar] [CrossRef] [PubMed]
  48. Durante-Yánez, E.V.; Martínez-Macea, M.A.; Enamorado-Montes, G.; Combatt Caballero, E.; Marrugo-Negrete, J. Phytoremediation of soils contaminated with heavy metals from gold mining activities using Clidemia sericea D. Don. Plants 2022, 11, 597. [Google Scholar] [CrossRef]
  49. Wang, F.Y.; Cheng, P.; Zhang, S.Q.; Zhang, S.W.; Sun, Y.H. Contribution of arbuscular mycorrhizal fungi and soil amendments to remediation of heavy metal-contaminated soil using sweet sorghum. Pedosphere 2022, 32, 844–855. [Google Scholar] [CrossRef]
  50. Martini, A.N.; Papafotiou, M.; Massas, I.; Chorianopoulou, N. Growing of the cretan therapeutic herb Origanum dictamnus in the urban gabric: The effect of substrate and cultivation site on plant growth and potential toxic element accumulation. Plants 2023, 12, 336. [Google Scholar] [CrossRef]
  51. Yang, D.J.; Zhu, H.W.; Liu, J.Q.; Zhang, Y.J.; Wu, S.; Xiong, J.B.; Wang, F.Y. Risk assessment of heavy metals in soils from four different industrial plants in a medium-sized city in north China. Toxics 2023, 11, 217. [Google Scholar] [CrossRef] [PubMed]
  52. Kapoor, D.; Singh, M.P.; Kaur, S.; Bhardwaj, R.; Zheng, B.S.; Sharma, A. Modulation of the functional components of growth, photosynthesis, and anti-oxidant stress markers in cadmium exposed Brassica juncea L. Plants 2019, 8, 260. [Google Scholar] [CrossRef] [PubMed]
  53. Zhang, Z.W.; Dong, Y.Y.; Feng, L.Y.; Deng, Z.L.; Xu, Q.; Tao, Q.; Wang, C.Q.; Chen, Y.E.; Yuan, M.; Yuan, S. Selenium enhances cadmium accumulation capability in two mustard family species—Brassica napus and B. juncea. Plants 2020, 9, 904. [Google Scholar] [CrossRef] [PubMed]
  54. Liu, Y.Y.; Cui, W.Z.; Li, W.G.; Xu, S.; Sun, Y.H.; Xu, G.J.; Wang, F.Y. Effects of microplastics on cadmium accumulation by rice and arbuscular mycorrhizal fungal communities in Cd-contaminated soil. J. Hazard. Mater. 2023, 442, 130102. [Google Scholar] [CrossRef] [PubMed]
  55. Rizwan, M.; Noureen, S.; Ali, S.; Anwar, S.; Rehman, M.Z.U.; Qayyum, M.F.; Hussain, A. Influence of biochar amendment and foliar application of iron oxide nanoparticles on growth, photosynthesis, and cadmium accumulation in rice biomass. J. Soil. Sedim. 2019, 19, 3749–3759. [Google Scholar] [CrossRef]
  56. Han, Y.; Zveushe, O.K.; Dong, F.Q.; Ling, Q.; Chen, Y.; Sajid, S.; Zhou, L.; de Dios, V.R. Unraveling the effects of Arbuscular mycorrhizal fungi on cadmium uptake and detoxification mechanisms in perennial ryegrass (Lolium perenne). Sci. Total Environ. 2021, 798, 149222. [Google Scholar] [CrossRef] [PubMed]
  57. An, T.T.; Wu, Y.J.; Xu, B.C.; Zhang, S.Q.; Deng, X.P.; Zhang, Y.; Siddique, K.H.M.; Chen, Y.L. Nitrogen supply improved plant growth and Cd translocation in maize at the silking and physiological maturity under moderate Cd stress. Ecotoxicol. Environ. Safe 2022, 230, 113137. [Google Scholar] [CrossRef]
  58. Ghorbani, M.; Konvalina, P.; Neugschwandtner, R.W.; Kopecky, M.; Amirahmadi, E.; Moudry, J.; Mensik, L. Preliminary findings on cadmium bioaccumulation and photosynthesis in rice (Oryza sativa L.) and maize (Zea mays L.) using biochar made from C3- and C4-originated straw. Plants 2022, 11, 1424. [Google Scholar] [CrossRef]
  59. Esringu, A.; Turan, M.; Cangonul, A. Remediation of Pb and Cd polluted soils with fulvic acid. Forests 2021, 12, 1608. [Google Scholar] [CrossRef]
  60. Placido, D.F.; Lee, C.C. Potential of industrial hemp for phytoremediation of heavy metals. Plants 2022, 11, 595. [Google Scholar] [CrossRef]
  61. Deng, X.J.; Lu, L.L.; Li, H.W.; Luo, F. The adsorption properties of Pb(II) and Cd(II) on functionalized graphene prepared by electrolysis method. J. Hazard. Mater. 2010, 183, 923–930. [Google Scholar] [CrossRef] [PubMed]
  62. Yang, K.; Chen, B.; Zhu, X.; Xing, B. Aggregation, adsorption, and morphological transformation of graphene oxide in aqueous solutions containing different metal cations. Environ. Sci. Technol. 2016, 50, 11066–11075. [Google Scholar] [CrossRef] [PubMed]
  63. Bloor, J.M.; Handy, R.D.; Awan, S.A.; Jenkins, D.F.L. Graphene oxide biopolymer aerogels for the removal of lead from drinking water using a novel nano-enhanced ion exchange cascade. Ecotoxicol. Environ. Safe 2021, 208, 111422. [Google Scholar] [CrossRef] [PubMed]
  64. Deng, X.; Liu, R.; Hou, L. Promotion effect of graphene on phytoremediation of Cd-contaminated soil. Environ. Sci. Pollut. Res. 2022, 29, 74319–74334. [Google Scholar] [CrossRef] [PubMed]
  65. Cao, K.S.; Tian, Z.S.; Zhang, X.Y.; Wang, Y.B.; Zhu, Q.X. Green preparation of graphene oxide nanosheets as adsorbent. Sci. Rep. 2023, 13, 9314. [Google Scholar] [CrossRef]
  66. Thanabhorn, S.; Jaijoy, K.; Thamaree, S.; Ingkaninan, K.; Panthong, A. Acute and subacute toxicity study of the ethanol extract from Lonicera japonica Thunb. J. Ethnopharmacol. 2006, 107, 370–373. [Google Scholar] [CrossRef]
  67. Baker, A.J.M.; Brooks, R.R. Terrestrial higher plants which hyperaccumulate metallic elements- a review of their distribution, ecology and phytochemistry. Biorecovery 1989, 1, 81–126. [Google Scholar]
  68. Liu, Z.L.; Chen, W.; He, X.Y. Cadmium-induced changes in growth and antioxidative mechanisms of a medicine plant (Lonicera japonica Thunb.). J. Med. Plants Res. 2011, 5, 1411–1417. [Google Scholar]
  69. Liu, Z.L.; He, X.Y.; Chen, W.; Yuan, F.H.; Yan, K.; Tao, D.L. Accumulation and tolerance characteristics of cadmium in a potential hyperaccumulator—Lonicera japonica Thunb. J. Hazard. Mater. 2009, 169, 170–175. [Google Scholar] [CrossRef]
  70. Liu, Z.L.; He, X.Y.; Chen, W. Effects of cadmium hyperaccumulation on the concentrations of four trace elements in Lonicera japonica Thunb. Ecotoxicology 2011, 20, 698–705. [Google Scholar] [CrossRef]
  71. Liu, Z.L.; Chen, W.; He, X.Y.; Jia, L.; Huang, Y.Q.; Zhang, Y.; Yu, S. Cadmium-induced physiological response in Lonicera japonica Thunb. Clean-Soil Air Water 2013, 41, 478–484. [Google Scholar] [CrossRef]
  72. Liu, Z.L.; Chen, W.; He, X.Y. Influence of Cd2+ on growth and chlorophyll fluorescence in a hyperaccumulator—Lonicera japonica Thunb. J. Plant Growth Regul. 2015, 34, 672–676. [Google Scholar] [CrossRef]
  73. Liu, Z.; Chen, W.; He, X.; Jia, L.; Yu, S.; Zhao, M. Hormetic responses of Lonicera Japonica Thunb. to cadmium stress. Dose-Response 2015, 13, 1–10. [Google Scholar] [CrossRef]
  74. Liu, Z.L.; Chen, Q.L.; Lin, M.S.; Chen, M.D.; Zhao, C.; Lu, Q.X.; Meng, X.Y. Electric field-enhanced cadmium accumulation and photosynthesis in a woody ornamental hyperaccumulator—Lonicera japonica Thunb. Plants 2022, 11, 1040. [Google Scholar] [CrossRef] [PubMed]
  75. Chen, L.; Hu, W.F.; Long, C.; Wang, D. Exogenous plant growth regulator alleviate the adverse effects of U and Cd stress in sunflower (Helianthus annuus L.) and improve the efficacy of U and Cd remediation. Chemosphere 2021, 262, 127809. [Google Scholar] [CrossRef] [PubMed]
  76. Yin, L.Y.; Wang, Z.; Wang, S.G.; Xu, W.Y.; Bao, H.F. Effects of graphene oxide and/or Cd2+ on seed germination, seedling growth, and uptake to Cd2+ in solution culture. Water Air Soil Pollut. 2018, 229, 151. [Google Scholar] [CrossRef]
  77. He, Y.J.; Qian, L.C.; Zhou, K.; Hu, R.R.; Huang, M.R.; Wang, M.; Zhao, G.K.; Liu, Y.L.; Xu, Z.P.; Zhu, H.W. Graphene oxide promoted cadmium uptake by rice in soil. ACS Sustain. Chem. Eng. 2019, 7, 10283–10292. [Google Scholar] [CrossRef]
  78. Yang, L.; Chen, Y.; Shi, L.; Yu, J.; Yao, J.; Sun, J.; Zhao, L.; Sun, J. Enhanced Cd accumulation by graphene oxide (GO) under Cd stress in duckweed. Aquat. Toxicol. 2020, 229, 105579. [Google Scholar] [CrossRef]
  79. Jin, Z.; Wang, X.; Sun, Y.; Ai, Y.; Wang, X. Adsorption of 4-n-nonylphenol and bisphenol-A on magnetic reduced graphene oxides: A combined experimental and theoretical studies. Environ. Sci. Technol. 2015, 49, 9168–9175. [Google Scholar] [CrossRef]
  80. Lingamdinne, L.P.; Koduru, J.; Roh, H.; Choi, Y.L.; Chang, Y.Y.; Yang, J.K. Adsorption removal of Co(II) from waste-water using graphene oxide. Hydrometallurgy 2016, 165, 90–96. [Google Scholar] [CrossRef]
  81. Gong, X.M.; Huang, D.L.; Liu, Y.G.; Peng, Z.W.; Zeng, G.M.; Xu, P.; Cheng, M.; Wang, R.Z.; Wan, J. Remediation of contaminated soils by biotechnology with nanomaterials: Bio-behavior, applications, and perspectives. Crit. Rev. Biotechnol. 2017, 38, 455–468. [Google Scholar] [CrossRef] [PubMed]
  82. Abbasi, H.; Pourmajidian, M.R.; Hodjati, S.M.; Fallah, A.; Nath, S. Effect of soil-applied lead on mineral contents and biomass in Acer cappadocicum, Fraxinus excelsior and Platycladus orientalis seedlings. iForest 2017, 10, 722–728. [Google Scholar] [CrossRef]
  83. Siddique, A.B.; Rahman, M.M.; Islam, M.R.; Mondal, D.; Naidu, R. Response of iron and cadmium on yield and yield components of rice and translocation in grain: Health risk estimation. Front. Environ. Sci. 2021, 9, 716770. [Google Scholar] [CrossRef]
  84. Liu, Z.L.; Tian, L.; Chen, M.D.; Zhang, L.H.; Lu, Q.X.; Wei, J.B.; Duan, X.B. Hormesis responses of growth and photosynthetic characteristics in Lonicera japonica Thunb. to cadmium stress: Whether electric field can improve or not? Plants 2023, 12, 933. [Google Scholar] [CrossRef] [PubMed]
  85. Aery, N.C.; Rana, D.K. Growth and cadmium uptake in barley under cadmium stress. J. Environ. Biol. 2003, 24, 117–123. [Google Scholar] [PubMed]
  86. Ruiz, O.N.; Fernando, K.A.S.; Wang, B.; Brown, N.A.; Luo, P.G.; Mcnamara, N.D.; Vangsness, M.; Sun, Y.P.; Bunker, C.E. Graphene oxide: A nonspecific enhancer of cellular growth. ACS Nano 2011, 5, 8100–8107. [Google Scholar] [CrossRef] [PubMed]
  87. Guo, X.; Mei, N. Assessment of the toxic potential of graphene family nanomaterials. J. Food Drug Anal. 2014, 22, 105–115. [Google Scholar] [CrossRef]
  88. Kabiri, S.; Degryse, F.; Tran, D.N.; Da Silva, R.C.; McLaughlin, M.J.; Losic, D. Graphene oxide: A new carrier for slow release of plant micronutrients. ACS Appl. Mater. Interfaces 2017, 9, 43325–43335. [Google Scholar] [CrossRef]
  89. Abbas, T.; Nadeem, M.A.; Tanveer, A.; Chauhan, B.S. Can hormesis of plant- released phytotoxins be used to boost and sustain crop production? Crop Protect. 2017, 93, 69–76. [Google Scholar] [CrossRef]
  90. Kim, S.A.; Lee, Y.M.; Choi, J.Y.; Jacobs, D.R., Jr.; Lee, D.H. Evolutionarily adapted hormesis-inducing stressors can be a practical solution to mitigate harmful effects of chronic exposure to low dose chemical mixtures. Environ. Pollut. 2018, 233, 725–734. [Google Scholar] [CrossRef]
  91. Agathokleous, E.; Calabrese, E.J. Hormesis can enhance agricultural sustainability in a changing world. Glob. Food Secur. 2019, 20, 150–155. [Google Scholar] [CrossRef]
  92. Agathokleous, E.; Calabrese, E.J. Hormesis: The dose response for the 21st century: The future has arrived. Toxicology 2019, 425, 152249. [Google Scholar] [CrossRef] [PubMed]
  93. Agathokleous, E.; Kitao, M.; Calabrese, E.J. Hormetic dose responses induced by lanthanum in plants. Environ. Pollut. 2019, 244, 332–341. [Google Scholar] [CrossRef] [PubMed]
  94. Erofeeva, E.A. Environmental hormesis of non-specific and specific adaptive mechanisms in plants. Sci. Total Environ. 2022, 804, 150059. [Google Scholar] [CrossRef] [PubMed]
  95. Haque, A.M.; Tasnim, J.; El-Shehawi, A.M.; Rahman, M.A.; Parvez, M.S.; Ahmed, M.B.; Kabir, A.H. The Cd-induced morphological and photosynthetic disruption is related to the reduced Fe status and increased oxidative injuries in sugar beet. Plant Physiol. Biochem. 2021, 166, 448–458. [Google Scholar] [CrossRef]
  96. Huang, X.Y.; Fan, C.W.; Xie, D.Y.; Chen, H.X.; Zhang, S.; Chen, H.; Qin, S.; Fu, T.L.; He, T.B.; Gao, Z.R. Synergistic effects of water management and silicon foliar spraying on the uptake and transport efficiency of cadmium in rice (Oryza sativa L.). Plants 2023, 12, 1414. [Google Scholar] [CrossRef]
  97. Chen, L.Y.; Yang, S.N.; Liu, Y.; Mo, M.; Guan, X.; Huang, L.; Sun, C.; Yang, S.T.; Chang, X.L. Toxicity of graphene oxide to naked oats (Avena sativa L.) in hydroponic and soil cultures. RSC Adv. 2018, 8, 15336–15343. [Google Scholar] [CrossRef]
  98. Zhao, S.L.; Zhu, X.G.; Mou, M.D.; Wang, Z.Y.; Duo, L. Assessment of graphene oxide toxicity on the growth and nutrient levels of white clover (Trifolium repens L.). Ecotoxicol. Environ. Safe 2022, 234, 113399. [Google Scholar] [CrossRef]
  99. De Marchi, L.; Neto, V.; Pretti, C.; Figueira, E.; Brambilla, L.; Rodriguez-Douton, M.J.; Rossella, F.; Tommasini, M.; Furtado, C.; Soares, A.M.V.M.; et al. Physiological and biochemical impacts of graphene oxide in polychaetes: The case of Diopatra neapolitana. Comp. Biochem. Phys. C 2017, 193, 50–60. [Google Scholar] [CrossRef]
  100. Hazeem, L.J.; Bououdina, M.; Dewailly, E.; Slomianny, C.; Barras, A.; Coffinier, Y.; Szunerits, S.; Boukherroub, R. Toxicity effect of graphene oxide on growth and photosynthetic pigment of the marine alga Picochlorum sp. during different growth stages. Environ. Sci. Pollut. Res. 2017, 24, 4144–4152. [Google Scholar] [CrossRef]
  101. Zhou, Z.X.; Li, J.X.; Li, C.; Guo, Q.; Hou, X.C.; Zhao, C.Q.; Wang, Y.; Chen, C.S.; Wang, Q.H. Effects of graphene oxide on the growth and photosynthesis of the emergent plant Iris pseudacorus. Plants 2023, 12, 1738. [Google Scholar] [CrossRef] [PubMed]
  102. Pietrini, F.; Zacchini, M.; Iori, V.; Pietrosanti, L.; Bianconi, D.; Massacci, A. Screening of poplar clones for cadmium phytoremediation using photosynthesis, biomass and cadmium content analyses. Int. J. Phytoremediat. 2009, 12, 105–120. [Google Scholar] [CrossRef] [PubMed]
  103. Jin, S.S.; Zhang, E.R.; Guo, H.T.; Hu, C.W.; Zhang, Y.R.; Yan, D.F. Comprehensive evaluation of carbon sequestration potential of landscape tree species and its influencing factors analysis: Implications for urban green space management. Carbon Bal. Manag. 2023, 18, 17. [Google Scholar] [CrossRef] [PubMed]
  104. Nascentes, R.F.; Carbonari, C.A.; Simoes, P.S.; Brunelli, M.C.; Velini, E.D.; Duke, S.O. Low doses of glyphosate enhance growth, CO2 assimilation, stomatal conductance and transpiration in sugarcane and eucalyptus. Pest Manag. Sci. 2018, 74, 1197–1205. [Google Scholar] [CrossRef] [PubMed]
  105. Zhang, H.; Wang, L. Species diversity and carbon sequestration oxygen release capacity of dominant communities in the Hancang river basin, China. Sustainability 2022, 14, 5405. [Google Scholar] [CrossRef]
  106. Berg, I.A. Ecological aspects of the distribution of different autotrophic CO2 fixation pathways. Appl. Environ. Microbiol. 2011, 77, 1925–1936. [Google Scholar] [CrossRef]
  107. Zhang, J.; Shi, Y.J.; Zhu, Y.Q.; Liu, E.B.; Li, M.; Zhou, J.P.; Li, J.G. The photosynthetic carbon fixation characteristics of common tree species in northern Zhejiang. Acta Ecol. Sin. 2013, 33, 1740–1750. [Google Scholar] [CrossRef]
Plants 13 00019 g001
Figure 1. The effect of different GO-Cd treatments on Cd contents in root and shoots of L. japonica. The “**” indicates a significant difference compared with the control (p < 0.01), and the “*” indicates a significant difference compared with the control (p < 0.05). Mean ± SD.
Figure 1. The effect of different GO-Cd treatments on Cd contents in root and shoots of L. japonica. The “**” indicates a significant difference compared with the control (p < 0.01), and the “*” indicates a significant difference compared with the control (p < 0.05). Mean ± SD.
Plants 13 00019 g001
Plants 13 00019 g002
Figure 2. The effect of different GO-Cd treatments on root and shoots biomass dry weight (g) of L. japonica. The “**” indicates a significant difference compared with the control (p < 0.01), and the “*” indicates a significant difference compared with the control (p < 0.05). Mean ± SD.
Figure 2. The effect of different GO-Cd treatments on root and shoots biomass dry weight (g) of L. japonica. The “**” indicates a significant difference compared with the control (p < 0.01), and the “*” indicates a significant difference compared with the control (p < 0.05). Mean ± SD.
Plants 13 00019 g002
Plants 13 00019 g003
Figure 3. The effect of different GO-Cd treatments on net photosynthesis rate (Pn) in L. japonica. Mean ± SD.
Figure 3. The effect of different GO-Cd treatments on net photosynthesis rate (Pn) in L. japonica. Mean ± SD.
Plants 13 00019 g003
Table 1. Different experimental treatments.
Table 1. Different experimental treatments.
Test NumberGO-Cd TreatmentsGO Concentration
in Solution (mg L−1)		Cd Concentration
in Solution (mg L−1)
T1GO0-Cd000
T2GO0-Cd505
T3GO0-Cd25025
T4GO10-Cd0100
T5GO10-Cd5105
T6GO10-Cd251025
T7GO50-Cd0500
T8GO50-Cd5505
T9GO50-Cd255025
T10GO100-Cd01000
T11GO100-Cd51005
T12GO100-Cd2510025
Table 2. The effect of different GO-Cd treatments on the carbon sequestration and oxygen release characteristics of L. japonica.
Table 2. The effect of different GO-Cd treatments on the carbon sequestration and oxygen release characteristics of L. japonica.
Test NumberGO-Cd TreatmentsCarbon Sequestration Per Unit Leaf Area (g m−2 d−1)Oxygen Release Per Unit Leaf Area (g m−2 d−1)
T1GO0-Cd010.13 ± 0.267.37 ± 0.14
T2GO0-Cd512.06 ± 0.31 *8.77 ± 0.28 *
T3GO0-Cd2511.28 ± 0.25 8.20 ± 0.33
T4GO10-Cd013.04 ± 0.53 **9.48 ± 0.21 **
T5GO10-Cd516.75 ± 0.42 **12.18 ± 0.35 **
T6GO10-Cd2514.62 ± 0.17 10.63 ± 0.29
T7GO50-Cd012.39 ± 0.31 * 9.01 ± 0.50 *
T8GO50-Cd515.17 ± 0.16 **11.03 ± 0.41 **
T9GO50-Cd2513.41 ± 0.37 9.75 ± 0.18
T10GO100-Cd011.25 ± 0.29 8.18 ± 0.36
T11GO100-Cd514.08 ± 0.33 * 10.24 ± 0.25 *
T12GO100-Cd2512.19 ± 0.24 8.87 ± 0.19
The “**” indicates a significant difference compared with the control (p < 0.01), and the “*” indicates a significant difference compared with the control (p < 0.05). Mean ± SD.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Liu, Z.; Lu, Q.; Zhao, Y.; Wei, J.; Liu, M.; Duan, X.; Lin, M. Ameliorating Effects of Graphene Oxide on Cadmium Accumulation and Eco-Physiological Characteristics in a Greening Hyperaccumulator (Lonicera japonica Thunb.). Plants 2024, 13, 19. https://doi.org/10.3390/plants13010019

AMA Style

Liu Z, Lu Q, Zhao Y, Wei J, Liu M, Duan X, Lin M. Ameliorating Effects of Graphene Oxide on Cadmium Accumulation and Eco-Physiological Characteristics in a Greening Hyperaccumulator (Lonicera japonica Thunb.). Plants. 2024; 13(1):19. https://doi.org/10.3390/plants13010019

Chicago/Turabian Style

Liu, Zhouli, Qingxuan Lu, Yi Zhao, Jianbing Wei, Miao Liu, Xiangbo Duan, and Maosen Lin. 2024. "Ameliorating Effects of Graphene Oxide on Cadmium Accumulation and Eco-Physiological Characteristics in a Greening Hyperaccumulator (Lonicera japonica Thunb.)" Plants 13, no. 1: 19. https://doi.org/10.3390/plants13010019

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop