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Article Cite This: ACS Omega 2018, 3, 17770−17777
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Carbon Nanodots for Enhancing the Stress Resistance of Peanut Plants Li-Xia Su,†,§,∥ Xing-Li Ma,‡,∥ Kun-Kun Zhao,‡ Cheng-Long Shen,† Qing Lou,*,† Dong-Mei Yin,*,‡ and Chong-Xin Shan*,† †
Key Laboratory of Diamond Optoelectronic Materials and Devices, School of Physics and Engineering, Zhengzhou University, Zhengzhou 450052, China ‡ College of Agronomy, Henan Agricultural University, Zhengzhou 450002, China § College of Science, Henan University of Engineering, Zhengzhou 451191, China
ACS Omega 2018.3:17770-17777. Downloaded from pubs.acs.org by 95.85.80.189 on 01/06/19. For personal use only.
S Supporting Information *
ABSTRACT: Herein, the effect of carbon nanodots (CDs) on the stress resistance of peanuts has been studied. It is found that the stress-resistance ability of peanut plants can be enhanced significantly when cultivated in CD aqueous solution with optimal concentration. Because of the increased stress-resistance ability, the growth of peanut plants can be boosted, and the output of the peanuts can be increased by about 9%. Confocal fluorescence images showed that the CDs can be transferred from the roots to leaves through the xylem vessels of the peanut plants. The existence of hydrophilic radical groups on the surface of CDs may result in largely retaining and slowly releasing micronutrients inside the xylem vessels of the peanuts, further guaranteeing the supply of essential nutrients required for peanuts and boosting the stress-resistance ability of the peanuts.
1. INTRODUCTION
of nanomaterials is essential due to their potential endangering effect for living organisms on the earth.18 Recently, one of these nanocarbon materials, carbon nanodots (CDs), have attracted much attention due to their fantastic potential applications in bioimaging, sensors, optoelectronics, energy devices, security ink, and so on;19−23 especially great progress has been achieved in the synthetic method and photoelectric properties.24−26 In addition, some researchers have explored the effect of CDs on the growth of plants. Li et al. performed the uptake kinetics study of CDs in the plant system and demonstrated that the CDs imposed no phytotoxicity on mung bean growth.6 Sarkar et al. found that proper concentration of CDs could stimulate the growth of wheat due to its capacity for holding the nutrient ions.27 Nevertheless, the effect of CDs on stress resistance of plants has not been studied yet, which is closely correlated with the growth and productivity of plants. In fact, the crop productivity is affected significantly by environmental factors, such as extreme temperatures, UV radiation, salinity, heavy metals, and so on, and more than 90% of the arable lands are under environmental stresses.28,29 Thus, it is of great significance to study the effect of the CDs on the stress resistance of plants. In this paper, the effect of CDs on the stress resistance of peanuts has been reported. Peanuts, as a major source of
Carbon, as one of the main components of organic materials, widely exists in natural lives. Recently, nanosized carbon materials have attracted considerable concerns for their unique physicochemical properties, such as high photostability, good biological compatibility, and low toxicity; these properties make nanocarbon materials have potential applications in bioimaging, sensing, photocatalysis, and optoelectronic devices,1−5 In recent years, several reports have demonstrated that some nanocarbon materials have influence on the growth and development process of plants.6−8 Lin et al. found a positive effect on germination and seedling of rice when treated with appropriate concentration of fullerene C70.9 Tan et al. suggested that multiwalled carbon nanotubes would increase reactive oxygen species and decrease the cell viability of rice plants.10 Khodakovskaya et al. demonstrated the use of carbon nanotubes to improve the growth of tobacco at an individual cell level.11 Miralles et al. used carbon nanotubes to study the phytotoxicity of wheat.12 In a subsequent study, Sonkar et al. found that proper concentration of water solution carbon nano-onions can enhance the production of gram plants.13 Furthermore, the effect of nanomaterials on plant stress resistance has also been studied. At appropriate dose, nanomaterials significantly suppress viral infection and proliferation as well as inhibit pathogen infection in plants. Therefore, certain nanomaterials have been used as herbicides and fungicides in agriculture.14−17 However, rational utilization © 2018 American Chemical Society
Received: September 30, 2018 Accepted: November 16, 2018 Published: December 19, 2018 17770
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Figure 1. (a) Transmission electron microscopy (TEM) image of the CDs, and the inset shows the high resolution TEM (HRTEM) image of the CDs; (b) XRD pattern of the CDs; (c) Raman spectrum of the CDs; (d) Fourier transform infrared (FTIR) spectrum of the CDs; (e) X-ray photoelectron spectrum (XPS) of the CDs, and the inset shows the C 1s spectra; (f) emission spectrum and excitation spectrum of the CDs monitored at 440 nm. The inset is the photographs of the CD solution taken under daylight and 365 nm irradiation conditions.
protein and vegetable oil for human nutrition (about 25% protein and 50% oil), have been employed as the sample plant since it is an important economic crop in the world.29 The peanut annual planting area in the world is around 24 million hectares, with an annual production of nearly 35 million tons.30 With the improvement of the living standard of humans, the demand for yield and quality of peanuts is increasing. Hence, it is urgent to boost peanut yield using many measures, including enhanced stress resistance, reasonable planting, and so on. Here, it is found that an optimized concentration of CDs can promote the stress resistance of peanut plants, and thanks to the enhanced stress-resistance ability, the growth and productivity of peanuts have been increased significantly compared with the reference samples. The reason for the enhanced stress resistance can be ascribed to the existence of hydrophilic radical groups on the surface of CDs, which may largely retain and slowly release micronutrients inside the xylem vessels of the peanuts.
Figure 2. Antidrought effect of CDs on peanut seedling.
mV and less than 10 nm, respectively, which imply the CDs have a good water solubility and cell penetrating ability (Figures S2 and S3). The X-ray diffractometer (XRD) pattern of the CDs exhibits a broad peak at around 23.4°, as shown in Figure 1b, which can be assigned to the graphite-like carbon structure.31 Figure 1c shows the Raman spectrum of the CDs, where the D band (at around 1347 cm−1) and G band (at around 1577 cm−1) can be attributed to the amorphous carbon and the graphite-structure carbon, respectively.32 To identify the elements in the CDs, the FTIR spectrum and XPS spectrum were collected. From the FTIR spectrum (Figure 1d), the broad band at 3150−3600 cm−1 can be assigned to the vibration absorption of O−H/N−H, the band
2. RESULTS AND DISCUSSION 2.1. Characterization of CDs. The morphology of the CDs was measured by TEM. As shown in Figure 1a, the CDs are well dispersed with size ranges from 2 to 5 nm, and the average size of the CDs is around 3.9 nm (Figure S1). The ζpotential and dynamic light scattering size of the CDs are 77 17771
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with two peaks at 300 and 365 nm, which is usually assigned to the n−π* transition of conjugated CO and CN.35 A broad emission appears at around 440 nm under the excitation of 365 nm. The inset of Figure 1f shows the image of the CD aqueous solution under daylight and UV light (365 nm) illumination conditions, and the solution is clear under daylight, but obvious blue fluorescence can be observed under 365 nm illumination conditions, which is consistent with the fluorescence spectrum that peaked at 440 nm. In addition, the cytotoxicity of CDs was measured, as shown in Figure S4. It shows that near 93% viability is obtained by incubating the A549 cells with the CDs for 48 h even at a high concentration of 500 μg/mL, which suggests that the CDs have a good biocompatibility and very low cytotoxicity at high concentration. 2.2. Effects of CDs on the Stress Resistance of Peanuts. The poly(ethylene glycol) (PEG) is widely used as an osmolyte in drought-related experiments. With molecular weight of 6000 g/mol, PEG molecules are small enough to influence the osmotic potential, but cannot be absorbed by plants. Meanwhile, they are inserted, nonpenetrating, watersolution, and nonionic polymers. So PEG-6000 has been frequently used to induce water stress and maintain a uniform water potential throughout the experimental period.36−39 The simulated drought stress experiment of the peanut is shown in Figure 2. The peanut plants treated by PEG-6000 (20%) exhibit obvious growth inhibition. However, the introduction of CDs can relieve the growth inhibition. The plants treated by only CDs (180 mg/L) grow best among these experimental plants. These results suggest that CDs act as a droughtresistant agent in the peanut growth process. To further understand the effect of the CDs on peanut plant growth, the direct uptake process of the CDs by the peanut seedlings was investigated by TEM, as shown in Figure 3. From the control check group (CK) treated with deionized water in Figure 3a, no obvious CDs can be found in the root
Figure 3. TEM images of peanut seedling roots cultured with deionized water (a), PEG (b), CDs (c), and PEG + CDs (d). The selected areas marked by red circles in (c) and (d) are CDs.
at 1600−1690 cm−1 to the stretching vibrations of CO/C C, and the band at around 1350−1390 cm−1 to the stretching vibrations of C−N.33 The XPS spectra of the CDs reveal the presence of C, N, and O, as shown in Figure 1e. The highresolution C 1s spectrum is shown in the inset of Figure 1e, and the spectrum can be fitted well using three Gaussian peaks, which can be attributed to C−O, C−C, and C−O−NH.33,34 The above results reveal the presence of amide and hydroxy groups on the surface of the CDs. Because of these groups, the CDs show hydrophilic characteristics and can be dispersed in aqueous solution well. The room-temperature fluorescence and excitation spectra of the aqueous CD solution are shown in Figure 1f. The excitation spectrum displays a broad spectrum
Figure 4. Activities of enzymes (a) SOD, (b) CAT, (c) POD, and (d) MDA at different growth periods. 17772
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Figure 5. Effect of CDs on the growth and development of peanut plants after cultivation for 15 days: (a) root activity, (b) root length, (c) root number, (d) seedling height, (e) dry weight, and (f) fresh weight of peanut plants grown in different concentrations of CDs.
POD activities and MDA content were measured to study the effect of the CDs on the antiaging process of peanut plants. The peanut plant seedlings were cultivated in aqueous solution with CD concentration of 180 mg/L for 15 days, and the CK groups were treated by deionized water under the same conditions. From Figure 4, it is seen that the peanut plants cultivated in CD solution have higher activities of SOD, CAT, and POD, with lower MDA content, compared with the CK groups, suggesting that the peanut plants cultivated in CD solution have better ability to remove active oxygen, thus reducing the membrane lipid peroxidation level and maintaining normal physiological function of the cells. These results suggest the peanut plant seedlings cultivated in CD solution seem to have stronger antioxidant enzymes and thus may better protect the plant from oxidative stress. From the above results, it is concluded that the stress resistance of peanuts can be enhanced by CDs, which is beneficial for the growth and productivity of peanuts. To confirm the prediction, the effects of CDs on the growth and yield of peanuts were investigated. 2.3. Effects of CDs on Peanut Plant Growth and Productivity. To study the effect of CDs on the growth of peanut plants, six beakers with CD concentrations of 0, 50, 130, 180, 250, and 500 mg/L have been employed as the
cells of the peanut plants. Similar results were obtained from Figure 3b, which was cultivated by PEG solution (20%). However, TEM images of the roots treated by 180 mg/L CDs obviously show the presence of CDs, and the CDs are agglomerated into clusters in the intercellular space of the root of the peanut plants, as shown in Figure 3c,d. The average diameter of the agglomerate CDs is in the range of ∼50 nm, which is smaller than the xylem vessels (usually several micrometers in diameter); thus, the CDs could easily drift inside the xylem vessel due to the potential drift caused by water suction through capillary action.6 The effect of CDs on the antiaging process of peanut plants was also determined, which maintained a positive correlation with the plants’ stress resistance. The activity of relative enzymes is usually used to characterize the aging of plants. The superoxide dismutase (SOD) activity marks the strength of a plant cell’s ability to resist aging. The catalase (CAT) and peroxidase (POD) activities can provide protective effects on cells by eliminating free radicals and increasing metabolism. Malonaldehyde (MDA) is one of the peroxide metabolites in plants that can damage the cell membranes.40−42 Generally, the increased activities of SOD, POD, and CAT will inhibit the production of MDA. Therefore, in this paper, SOD, CAT, and 17773
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constrained. Among the CD-treated plants, the best result is observed when the concentration of CDs is 180 mg/L. The root activity of the peanut plants cultivated in optimal CD concentration (180 mg/L) is 3.5 times larger than that of the control sample. In addition, the root length, seedling height, root number, root dry weight, shoot dry weight, root fresh weight, and shoot fresh weight are about 1.5 times of the corresponding values of the control sample. To show the promotion of growth of peanuts by the CDs more vividly, the images of the peanuts cultivated in optimal CD concentration (180 mg/L) and deionized water after cultivation for 15 days are shown in Figure 6. Obviously, the leaves and roots of the plants cultivated in CD solution are longer and thicker than those of the control sample, confirming that the CDs can promote the growth of peanut plants. The growth promotion effect of CDs on peanuts in natural soil conditions was also investigated. Similarly, the seedling with CDs exhibits an enhanced growth trend. Four months later, peanut plants irrigated with CDs had an increased fruit productivity, as shown in Figure 7. Compared with the CK sample, the pod number of 0.5 kg and seed number of 0.25 kg of peanut plants with CDs treatment are lower than those of the CK sample, indicating the weight per pod increased when the peanut plants were treated with CD solution during their growth process. The 100-pod weight and 100-seed weight of the peanut plants with CD treatment are higher than those of the CK sample, suggesting that the seeds obtained from plants cultivated with CD treatment have better plumpness. The shelling percentage of the peanuts with CD treatment (76.6%) is higher than that of the CK sample (76.1%), which further proves that the CDs have the function of promoting the growth of peanuts. The increase in the yield per Mu is also given, as shown in Figure 7. The yield per Mu of peanuts with CD treatment is 326.7 kg, which is 20 kg higher than that of the CK samples, indicating that the CDs can enhance the productivity of peanuts. The above results confirm that the growth and productivity of peanuts can be enhanced by CDs. The peanut seeds from the plant cultivated by CDs contain no CDs (Figure S6), which suggests that CDs may have no threat to food security. 2.4. Analysis of the Interaction between CDs and Peanuts. The interaction of CDs with peanut plants may follow several pathways as predicted for nanoparticle association and uptake in plants.13,43−47 The CDs may be sorbed onto the peanut surfaces and be taken up through natural nano- or micrometer-scale plant openings. Then, during the transportation of water and nutrient elements, the CDs can enter the xylem and phloem vessels of the plant. To understand the transmitting procedure and physical status of the CDs inside peanuts, the roots and leaves of peanut plants cultivated in CD solution for 15 days were analyzed by laser scanning microscopy (LSM). Before analysis, the peanut plants were cleaned thoroughly with deionized water. The control experiment suggests that CDs could be uptaken by the root cells of peanuts, as shown in Figure S7. According to the sections of roots (Figure 8a−c) and leaves (Figure 8d−f), the uptake of CDs by the root of peanut plants can be identified in vivo due to the strong blue fluorescence from the CDs, and accumulation of CDs in leaves can also be observed under excitation of 364 nm line of a lamp. The bright-field images of roots and leaves were also investigated and overlaid with the luminescence images. The results suggest that the CDs can enter plants and then were transferred to other parts of the
Figure 6. Leaf and root images of peanut seedlings treated by optimal concentration of CDs (180 mg/L) and deionized water (CK) after cultivation for 15 days.
Figure 7. Effect of CDs (180 mg/L) on the production of peanuts. (1) Pod number per 0.5 kg (No.). (2) Seed number per 0.25 kg (No.). (3) 100-Pod weight (g). (4) 100-Seed weight (g). (5) Shelling percentage (%). (6) Seed weight per 0.5 kg pods (g). (7) Yield per Mu (kg). (Note: Mu, a Chinese unit of area. 1 acre is approximately equal to 6.07 Mu, and 1 Mu is approximately equal to 667 m2.)
culture box. On increasing the concentration of the CDs, peanut seeds exhibit an increasing germination rate at relatively low CD concentration (Figure S5). As evidenced from the figure, the growth of peanut seeds can be promoted by the CDs. To study the effect of CDs on the growth of peanut plants further, some growth indicators, such as root activity, root length, root number, seeding height, shoot dry weight, and root−shoot ratio, were recorded after the peanuts were cultivated for 15 days, as shown in Figure 5. From this figure, one can see that the introduction of CDs can clearly increase the overall growth of peanut seedlings compared with the control sample. However, when the concentration of CDs is higher than a certain value, the growth of peanuts will be 17774
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Figure 8. LSM images of transverse sections and longitudinal sections from root and leaf of peanut plants, cultured with CDs (180 mg/L) for 15 days. (a) and (b) are the cross sections of the root under 364 nm light irradiation and bright field, respectively; (c) is the overlay of (a) and (b); (d) and (e) are the cross sections of the leaf under 364 nm light irradiation and bright field, respectively; and (f) is the overlay of (d) and (e). Note that all the images were collected under the same exposure conditions.
ultrasonically treated for 1 h and then transferred into a 150 mL Teflon-lined stainless steel autoclave. After being heated at 180 °C for 5 h, the autoclave was naturally cooled. Then, the obtained solution was further purified by using a 500 D dialysis for 8 h. The extracting solution was dried by using a vacuum freeze-drying method. CDs with concentrations of 0, 50, 130, 180, 250, and 500 mg/L were obtained by dissolving the CD powder in various amounts of deionized water. 4.3. Plant Growth. 4.3.1. Optimal Concentration Exploration Experiment. After being treated by water and sodium hypochlorite, peanut seeds (Nongda hua No.103, which was cultivated by professor Yin) with uniform size were placed into five glass bottles with a diameter of 10 cm, with 20 seeds in each bottle. First, 20 mL of CD solution was employed as the culture medium with CD concentrations of 50, 130, 180, 250, and 500 mg/L, separately. The control experiment was carried out in the same conditions except that the culture medium was replaced by deionized water. All the peanut seeds were placed in the illumination incubator under the irradiation of simulated sunlight for 8 h every day, and the temperature in the incubator was kept at 25 °C. 4.3.2. Drought-Resistance Experiment. After being treated by water and sodium hypochlorite, plump peanut seeds with uniform size were placed in a dark incubator at 25 °C. After 5 days, uniform seedlings were transferred into an illumination incubator with Hoagland nutrient solution. When the peanut seedlings grow to three leaves, the seedlings were transferred into setting experimental solution, and four experimental conditions were explored: blank control (only nutrient solution), CD solution (180 mg/L), poly(ethylene glycol) with a molecular weight of 6000 (PEG-6000) solution (20%), and PEG-6000 (20%) + CDs (180 mg/L). Four days later, the physiological properties of the seedlings were characterized. 4.3.3. Plant Growth in Natural Soil Conditions. The irrigation amount of the CDs (180 mg/L) was 10 L per plot (10 m2). The irrigation process can be divided into three stages: flowering period, 10 days after flowering, and 20 days after flowering. All peanuts irrigated with or without CD
peanut plants. The CDs can interact with the essential nutrients required for peanuts due to the existence of hydrophilic groups on CDs’ surface, which may largely retain and slowly release micronutrients inside the xylem vessels. In addition, these hydrophilic groups may help capture more water and reduce the moisture loss when the plants are in a dry environment, which can be caused by the compensation effect that appeared on drought stress after adding CDs in the field of peanuts. As a result, the growth and productivity of peanuts can be boosted with the irrigation of CD solutions due to the enhanced resistance to the harsh environments, which is unavoidable in a natural planting environment for peanuts.
3. CONCLUSIONS In summary, the effect of CDs on the stress resistance of peanuts was studied, and it was found that appropriate concentration of CD solutions will enhance the stress resistance of peanuts, and both growth and productivity of peanuts were improved with CD cultivation. The entire lifecycle stages of the peanut plants were monitored, and CDs show a positive effect in the growth progress of peanut plants. Considering the low cost, low toxicity, and abundance of CDs, the results reported in this paper may find a route to boost the growth and productivity of peanuts, one of the major economic crops in the world, and also may find a potential application field of CDs. 4. EXPERIMENTAL SECTION 4.1. Materials. The ammonium dihydrogen phosphate and citric acid used for the synthesis of the CDs were purchased from Sinopharm Chemical Reagent Co., Ltd. All the reagents were used without further purification, and deionized water was used in all the experiments. 4.2. Synthesis of Carbon Nanodots. The CDs were prepared via a hydrothermal method. Briefly, 2.1 g of citric acid was dissolved in 30.0 mL of water, and then 9.2 g of urea was added into the solution. Next, the obtained solution was 17775
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ACKNOWLEDGMENTS We gratefully acknowledge the support of this research by the National Natural Science Foundation of China (51602288, U1604263, 31471525, and U1704232), the Nature Foundation for Distinguished Young Scholars of China (61425021), the China Postdoctoral Science Foundation (2015M582192, 2016T90671), the key scientific and technological project in Henan Province (161100111000; S2012-05-G03).
solutions (180 mg/L) were harvested in 2017 from peanut crops grown at the Henan Agricultural University’s field station in Zhengzhou (E113°, N34°, 94 m altitude), China. Crops were cultivated and managed according to standard China agricultural practices involving an integrated pestmanagement scheme. 4.4. Activity Performance of Enzymes. The enzymatic activity of peanut sirrigated with or without CD solutions (180 mg/L) like superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), and malonaldehyde (MDA) were investigated at different growth periods (5, 15, and 25 days), respectively. All the activity analyses of enzymes were performed following the previous reports.48,49 4.5. Characterizations. The structural properties of the CDs were characterized by an X-ray diffractometer (XRD, PANational X′ Pert Pro). The Raman spectra were obtained on Raman spectrometers (Renishaw MR-2000) excited by the laser of 532 nm. Transmission electron microscope (TEM) and high resolution TEM (HRTEM) images were gained with a Technai G2 F20 microscope. X-ray photoelectron spectroscopy (XPS) spectrum was obtained by employing an X-ray photoelectron spectroscope (Axis Ultra DLD, Kratos). The Fourier transform infrared (FTIR) spectra were taken on a Nicolet Avatar 360 FTIR spectrophotometer. Photoluminescence spectra were recorded in an F-7000 Hitachi spectrometer. Laser scanning microscopy (LSM) was performed with LSM 710, Zeiss, equipped with 364 nm laser as the excitation source.
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REFERENCES
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acsomega.8b02604. Size distribution of the CDs (Figure S1); apparent ζpotential of the CDs in water measured by Zetasizer Nano ZS (Figure S2); particle size of CDs in water measured by Zetasizer Nano ZS (Figure S3); cell viability of A549 cells after 48 h incubation in the different concentration of CDs (Figure S4); effects of different concentrations of CDs on bud of peanut seeds after 1 day cultivation under the same condition, and contrast of the bud state of the peanuts seeding with optimal concentration of CDs and without CDs after 5 day cultivation (Figure S5); fluorescent emission spectrum of filter liquor of peanut powder aqueous solution (Figure S6) (PDF)
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AUTHOR INFORMATION
Corresponding Authors
*E-mail:
[email protected] (Q.L.). *E-mail:
[email protected] (D.-M.Y.). *E-mail:
[email protected] (C.-X.S.). ORCID
Qing Lou: 0000-0002-8852-8453 Author Contributions ∥
L.-X.S. and X.-L.M. contributed equally to this work.
Notes
The authors declare no competing financial interest. 17776
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DOI: 10.1021/acsomega.8b02604 ACS Omega 2018, 3, 17770−17777
