Efficacy of ABA-Mimicking Ligands in Controlling Water Loss and

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Cite This: J. Agric. Food Chem. XXXX, XXX, XXX−XXX

Efficacy of ABA-Mimicking Ligands in Controlling Water Loss and Maintaining Antioxidative Capacity of Spinacia oleracea Danying Ma,†,‡ Yong Xu,† Zhanquan Zhang,† Boqiang Li,† Tong Chen,*,† and Shiping Tian†,‡,§ †

Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China University of Chinese Academy of Sciences, Beijing 100049, China § Key Laboratory of Post-Harvest Handling of Fruits, Ministry of Agriculture, Beijing 100093, China ‡

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ABSTRACT: Abscisic acid (ABA) is a central regulator for various developmental processes and responses to abiotic stresses in plants. However, its practical application in controlling water loss of postharvest produces is largely restrained. Herein, the present study reported that two ABA-mimicking ligands, AM1 and AMF4, markedly reduced water loss by promoting stomatal closure and effectively alleviated weight loss in spinach. AM1 and AMF4 also alleviated chlorophyll and vitamin C degradation and simultaneously reduced hydrogen peroxide and malondialdehyde (MDA) production; moreover, both enzymatic and nonenzymatic systems involved in antioxidative capacity were activated. The expression levels of SoOST1, SoSLAC1, SoRCAR3, SoPYL5, SoNCED3, and SoAREB1 were also up-regulated. These findings indicate that AM1 and AMF4 are promising as novel means for reducing water loss, maintaining visual quality, delaying senescence, and extending shelf life in leafy vegetables. KEYWORDS: ABA-mimicking ligand, antioxidant activity, stomatal closure, visual quality, water loss

1. INTRODUCTION Water loss is a major cause for weight loss and quality deterioration of fresh produces at the postharvest stage,1,2 and it may also affect shelf life and nutritional quality, induce ripening and senescence in climacteric fruit, and finally reduce their commercial values.3 As a consequence, leafy vegetables may wilt after water loss approximately 3−5%.4 Therefore, it is crucial to reduce water loss from fresh produces at both preharvest and postharvest stages. Transpiration is the principal reason for water loss in fruit and vegetables,5,6 and the rates of water loss are affected by their shapes and structures, as well as environmental factors.4 Therefore, appropriate handling and distribution practices in combination with optimal conditions are crucial for preserving quality and reducing postharvest losses.7 Low storage temperatures, high relative humidity, and low O2 atmosphere can reduce water loss of tissues and extend postharvest life of fresh produces.1,8,9 However, these measures are not necessarily practicable, since some fresh produces of tropical and subtropical origin (e.g., mango, tomato, and cucumber) are chill-sensitive and may develop symptoms of chilling injuries at temperatures below thresholds.10 It was demonstrated that exogenous abscisic acid (ABA) inhibited water loss of postharvest romaine lettuce during storage.5 Besides, ABA has been used for keeping the freshness of postharvest flowers.11 Nevertheless, ABA has few applications in practices due to its chemical instability, high production expenses, and rapid catabolism by plant enzymes.12 Recently, studies reported that several ABA receptor agonists, such as AM1 and AMF4, displayed lasting effects in promoting stomatal closure and protecting plants from water loss.12,13 In addition, AM1 and AMF4 are chemically more stable than ABA. Therefore, it is envisioned that intervention of ABA signaling © XXXX American Chemical Society

using these ABA-mimicking ligands may contribute to reducing water loss and overcoming drought stress. In the present study, the efficacies of two ABA-mimicking ligands, AM1 and AMF4, in controlling water loss and maintaining visual quality in spinach were examined. After further measurements on hydrogen peroxide and malondialdehyde (MDA) contents as well as antioxidant capacity, it was demonstrated that both ABA-mimicking ligands can improve the antioxidative capacity in spinach and activate key genes involved in responses to drought stress. These results may further enrich the measures for intervening ABA signaling using small molecules, in order to help fresh produces resist abiotic stresses at the postharvest stage.

2. MATERIALS AND METHODS 2.1. Chemicals. AM1 and AMF4 were kindly provided by Prof. Jiankang Zhu, Shanghai Center for Plant Stress Biology, Chinese Academy of Sciences. They were dissolved in DMSO, prepared as stock solutions at 100 mM, and stored at −20 °C before further use. 2.2. Sample Preparation and Treatment. Spinach (Spinacia oleracea L.) seedlings in uniform size and maturity were harvested from orchards in Beijing, and only the seedlings without lesions or physical injuries were selected for experiments. The seedlings were sprayed with equivalent volumes of 0.01% DMSO (control), 10 μM ABA, 10 μM AM1, and 10 μM AMF4, naturally dried for 10 min, and then stored in plastic boxes (200 mm × 130 mm × 50 mm) before sampling. The boxes were kept in the dark at 25 ± 2 °C for 3 days. Each treatment was performed in triplicate, at 400 g per replicate, and the experiment was performed twice. Received: October 24, 2018 Revised: November 25, 2018 Accepted: December 7, 2018

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DOI: 10.1021/acs.jafc.8b05859 J. Agric. Food Chem. XXXX, XXX, XXX−XXX

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Journal of Agricultural and Food Chemistry

Figure 1. Effects of AM1 and AMF4 on visual appearance (A and C) and fresh weight loss (B) in spinach during storage. The experiments were performed in triplicates, and the data were represented by the means ± standard deviations. Treatments followed by different letters are statistically different by the Duncan’s multiple range (P < 0.05). 2.3. Determination of Weight Loss. All samples were weighed at the beginning of the experiments and at each sampling for every 24 h using a digital balance. Fresh weight losses were expressed as the percentages of weight losses relative to the original weights.14 2.4. Determination of Chlorophyll Content and Vitamin C Content. In total, 0.5 g of spinach leaves was ground and extracted in 5 mL of 80% acetone for 10 min. After filtration, the extract was metered to 25 mL with 80% acetone, and the total chlorophyll content was measured by determining the absorbance at 652 nm. The results are represented as miligrams per gram of fresh weight (FW).15 Vitamin C content was measured according to Goldenberg et al.16 Spinach leaves (2.5 g) were mixed with an appropriate volume of 2% oxalic acid, and then ground and filtered against muslin. After the debris was removed, the extract was diluted to a final volume of 25 mL with 2% oxalic acid. The 10 mL dilution was titrated with 0.1‰ 2,6-dichlorophenolindophenol sodium (DCIPS) until the solution turned to a rose pink color for 15 s. Afterward, calibration was performed with 1 mg mL−1 ascorbic acid for the 0.1‰ DCIPS solution. The results were expressed in milligrams of ascorbic acid equivalents per 100 g fresh weight (FW). 2.5. Determination of Stomatal Aperture, Stomatal Conductance, and Transpiration Rate. For observations on stomata, abaxial epidermal peels were detached from fresh spinach leaves and floated in sterile water. The numbers of open and closed stomata were determined under the microscope (Zeiss Axioskop 40, Germany).17 Three leaves were sampled from each of 10 plants, and 20 separate fields were analyzed in each leaf. In addition, the stomatal conductance and the transpiration rate were determined according to Teng et al.18 with minor modifications. Twenty fully expanded leaves at the same position of different seedlings were selected for the measurement using a Portable Gas Exchange Fluorescence System GFS-3000 (Walz, Germany). Leaves were inserted into the leaf chamber, and the measurements were carried out at 25 °C, 50% air humidity, and 380 ppm of CO2. 2.6. Determination of Hydrogen Peroxide and Malondialdehyde (MDA) Contents. Hydrogen peroxide content was determined according to the method described by Zhang et al.19

where 5 g of spinach leaves was homogenized with precooled 80% acetone followed by centrifugation at 12000g for 20 min at 4 °C. Afterward, 1 mL of supernatant was mixed with 0.1 mL of 10% titanium tetrachloride (in concentrated hydrochloric acid, v/v) and 0.2 mL of concentrated ammonia solution, and then the mixture was centrifuged at 12000g for 15 min at 4 °C. The precipitate was washed with cold acetone twice and dissolved in 3 mL of 2 M H2SO4, and the absorbance was determined at 410 nm. H2O2 content was expressed as micromoles per gram of FW. MDA was measured using the 2-thiobarbituric acid method.20 Spinach leaves (1 g) were homogenized in 5 mL of 0.1% (w/v) TCA and centrifuged at 10000g for 20 min at 4 °C. Then, 1 mL of supernatant was precipitated with 2 mL of 10% TCA containing 0.67% (w/v) 2-thiobarbituric acid, incubated on a boiling water bath for 20 min, and then immediately cooled on ice. After centrifugation at 10000g for 10 min at 4 °C, the absorbance of the supernatant was measured at 532 nm and the value for nonspecific absorption at 600 nm was subtracted. MDA content was expressed in micromoles per gram of FW. 2.7. Determination of Superoxide Dismutase and Peroxidase Activity. Superoxide dismutase (SOD) activity was determined according to Nomura et al.21 based on the ability of SOD to inhibit the reduction of nitroblue tetrazolium (NBT). Spinach leaves (0.5 g) were homogenized with 0.5 mL of 50 mM phosphate buffer (pH 7.8) on ice and then centrifuged at 12000g for 30 min at 4 °C. The supernatant was collected and used for enzymatic activity assay at 560 nm. A unit of SOD was defined as the amount of extract showing 50% inhibition on the reduction rate of NBT. Peroxidase (POD) activity was measured as described by Hu et al.22 with minor modifications. Spinach leaves (0.5 g) were exactly weighed and mixed with 0.5 mL of 0.1 M acetic acid and sodium acetate buffer (pH 5.5) containing 4% polyvinyl polypyrrolidone (PVPP) and 1% Triton X-100. The mixture was centrifuged at 12000g for 30 min at 4 °C, and the supernatant was collected and used for POD activity assay. The variation in absorbance at 470 nm was determined every 30 s using the spectrophotometer. B


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Figure 2. Stomatal closure following treatment of AM1 and AMF4. (A) Microscopic observations on stomata in spinach leaves. Blue arrows indicated open stomata, and red arrows indicated closed stomata; bars represented 10 μm. (B) Statistical analysis on the percentage of open stomata. (C) Effects of AM1 and AMF4 on transpiration rate and stomatal conductance. The data were represented by means ± standard deviations. Treatments followed by different letters are statistically different by the Duncan’s multiple range (P < 0.05). 2.8. Determination of Total Phenolic Content and Antioxidant Activity. In total, 1 g of spinach leaves was ground and mixed with 20 mL of 70% ethanol before ultrasonic extraction for 30 min. Afterward, the mixture was centrifuged at 12000g for 10 min at 4 °C, and the supernatant was collected and used for antioxidant activity assay. Total phenolic content was determined using Folin−Ciocalteau reagent according to the method described by Diamanti et al.23 where 3 mL of supernatant was fully mixed with 60 μL of Folin−Ciocalteau reagent and 180 μL of 2% (w/v) Na2CO3. After the solution rested at 25 °C for 30 min, the absorbance was measured at 765 nm; the experiments were performed in triplicates, and the results were expressed as micrograms gallic acid equivalents per 100 g of fresh weight. The free radical scavenging activity of spinach leaves was conducted as reported by Wu et al.20 where the 1 mL of supernatant as mentioned above was added to 2 mL of 4% DPPH solution (w/v)

and kept in dark at room temperature for 30 min. The absorbance was determined at 765 nm. All measurements were performed in triplicate. 2.9. Gene Expression Analysis. After homology-based searching against NCBI database for protein sequences of AtOST1, AtSLAC1, AtRCAR3, AtAREB1, AtNCED3, and AtPYL5, we identified the homologues in spinach by BLASTP, and the CDS sequences were used for designing the primers for RT-qPCR analysis. Total RNA was extracted from frozen spinach leaves (100 mg) using Trizol reagent (Tiangen, China), and reverse transcription was performed using a PrimeScript RT reagent kit and purified using gDNA eraser (TaKaRa, Dalian). For gene expression analysis, RT-qPCR was performed on a Step One Plus Real-Time PCR System (Applied Biosystems) using SYBR premix ex Taq (TaKaRa, Dalian). The procedures were as follows: predenaturation at 95 °C for 30 s, denaturation at 95 °C for 5 s, annealing and elongation at 60 °C for 30 s, at 40 cycles. 18S rRNA was used as the reference gene for normalization. Relative expression C


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Figure 3. Changes in chlorophyll (A) and vitamin C (B) contents in spinach following treatments with AM1 and AMF4. The experiments were performed in triplicates, and the data were represented by means ± standard deviations. Statistical significance was determined using Student’s ttest in different samples (*P < 0.05; **P < 0.01). levels were calculated using the 2−△△Ct method.24 Each treatment was performed in triplicate. 2.10. Statistical Analysis. Statistical analyses were performed using SPSS software (SPSS Inc., Chicago, IL, USA). The results were expressed as the mean ± standard deviation (SD). Significance for the differences in the data was analyzed by one-way ANOVA.

3A and B, both chlorophyll and vitamin C contents decreased during storage in all of the groups, whereas the decreases upon AM1 and AMF4 treatments were significantly milder than those in the control group, particularly on the third day. Given the variations in chlorophyll and vitamin C contents, the results demonstrated that AM1 and AMF4 postponed the deterioration in the intrinsic quality of spinach, which may be advantageous for maintaining nutritional quality and prolonging shelf life. 3.4. Variations in Antioxidant Capacity Following AM1 and AMF4 Treatments. To further study the substantial effects of AM1 and AMF4 on the antioxidative capacity of spinach, hydrogen peroxide and malondialdehyde (MDA) contents were measured. The hydrogen peroxide and MDA contents in spinach generally increased during storage (Figure 4A and B), but the increases following AM1 and AMF4 treatments were significantly milder compared to those in the control. In the present study, the variations in SOD and POD activities of spinach were also examined. The SOD activity in the control group declined rapidly, whereas those of the treatments were persistently maintained at relatively high levels; the SOD activities after AM1 and AMF4 treatments were comparable to that of ABA treatment (Figure 4C). In contrast, POD activity in both the control and the treatment groups continuously increased during storage, whereas the POD activity of the control was lower than those of the treatments (Figure 4D). These results implied that AM1 and AMF4 treatments maintained SOD and POD activities at high levels over the whole storage period and thus may alleviate oxidative injuries. Similarly, the antioxidative capacity of a nonenzymatic system was also determined, taking the total phenol content (TPC) and α,α-diphenyl-β-picrylhydrazyl (DPPH) free radical scavenging activity as examples. Generally, both TPC and DPPH exhibited decreasing patterns in all the samples. However, they were higher in the samples treated with AM1 and AMF4 in comparison to those in the control (Figure 4E and F). Coincidently, AM1 and AMF4 treatments also significantly improved total phenol content and free radical scavenging activity in spinach, which may contribute to the alleviation of oxidative injuries due to water loss. 3.6. Variations in Expression Levels of the Genes Related to Stomatal Movements and Drought Tolerance. Given that AM1 and AMF4 promoted stomatal closure and improved tolerance to water loss, we were prompted to

3. RESULTS 3.1. AM1 and AMF4 Alleviate Water Loss and Weight Decrease in S. oleracea. As shown in Figure 1, the spinach seedlings in the control group displayed apparent phenotypes for water loss on the second day upon harvesting. Though the fresh weights persistently decreased over the entire storage period in all of the groups, the weight loss in the control group was more significant compared to those after treatments with ABA, AM1, and AMF4. Further close-up observations showed that the spinach leaves in the control group shriveled obviously compared to their counterparts in the treatment groups with AM1 and AMF4. Moreover, the weight losses of the AM1 and AMF4 treatments were lower than those of the ABA treatment all the time during the experiments. These results showed that AM1 and AMF4 effectively alleviated fresh weight loss of spinach during storage and their efficacy was better than ABA at the same concentration. 3.2. Efficacy of AM1 and AMF4 on Stomatal Aperture, Stomatal Conductance, and Transpiration Rate. To further explore the underlying mechanism of AM1 and AMF4 in controlling water loss, stomatal aperture, stomatal conductance, and transpiration rate were measured. As shown in Figure 2A and B, it was evident that the open stomata in spinach leaves following AM1 and AMF4 treatments were significantly less than those in the control and ABA treatment, as the percentage of open stomata in the control group was about 67.82 ± 1.63%, whereas it decreased to 46.97 ± 0.43%, 33.94 ± 0.86%, and 14.36 ± 1.45% upon treatments with ABA, AM1, and AMF4, respectively. AM1 and AMF4 treatment also significantly reduced stomatal conductance (Gs) and the transpiration rate (Tr) of spinach leaves (Figure 2C), corresponding well with the phenotypes for induced stomatal closure. These results confirmed that AM1 and AMF4 promoted stomatal closure in harvested spinach. 3.3. Total Chlorophyll and Vitamin C Degradation Was Alleviated Following AM1 and AMF4 Treatments. To determine whether AM1 and AMF4 led to changes in the intrinsic quality of spinach, total chlorophyll and vitamin C contents were determined accordingly. As illustrated in Figure D


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Figure 4. Changes in hydrogen peroxide (A) and MDA (B) contents, SOD (C) and POD (D) activity, total phenol content (E), and free radical scavenging activity (F) in spinach. The experiments were performed in triplicates, and the data were represented by means ± standard deviations. Statistical significance was determined using Student’s t-test in different samples (*P < 0.05; **P < 0.01).

to improper handling at the retailing level, resulting in direct weight losses and poor visual and nutritional quality.1,2 Basically, transpiration is the principal cause for weight loss in leafy vegetables.6 In higher plants, it has been demonstrated that photosynthesis and transpiration rates of leaves are associated with the regulations by ABA on opening or closure of stomata.12,25 ABA is a phytohormone crucial for growth and responses to abiotic stresses in plants.26 Moreover, it plays a vital role in reducing water transpiration by promoting stomatal closure.27 It was reported that exogenous ABA application can maintain a higher chlorophyll content, lower fresh weight loss, and reduce the transpiration rate by promoting stomatal closure in postharvest lettuce.5 However, there are still some unsolved problems for ABA application, such as chemical instability, high expenses for production, and rapid catabolism by plant enzymes.12 AM1 and AMF4 are structurally modified ABA-

examine the variations in the expression of key genes involved in stomatal movements and drought tolerance conferred by ABA signaling (SoOST1, SoSLAC1, SoRCAR3, SoPYL5, SoNCED3, and SoAREB1). As shown in Figure 5, the expression levels of the genes related to stomatal movement, ABA perception and signaling, as well as drought tolerance were all up-regulated dramatically in spinach after treatments with AM1 and AMF4. These findings further supported the results for macroscopic phenotypes in alleviated water loss as well as reduced stomatal conductance (Gs) and transpiration rate (Tr).

4. DISCUSSION Most fruit, vegetables, and other fresh produces have high water contents (80−95%) at harvest, whereas water losses are major problems for them in the postharvest chain.4 It may be attributed to a wide variety of factors from growing conditions E


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Figure 5. Variations in gene expression levels of SoOST1 (A), SoSLAC1 (B), SoRCAR3 (C), SoAREB1 (D), SoNCED3 (E), and SoPYL5 (F) in spinach. The expression levels are calculated relative to the expression of 18S rRNA. The experiments were performed in triplicates, and the data were represented by means ± standard deviations. Statistical significance was determined using Student’s t-test in different samples (**P < 0.01).

pattern (PAMP) treatment.29 Consequently, the elevated SoOST1, SoSLAC1, and SoRCAR3 expression may subsequently lead to stomatal closure, which was consistent with the results from microscopic observations on stomata. Compared to the control, the expression levels of SoPYL5, SoNCED3, and SoAREB1 were also up-regulated. Previous studies showed that overexpression of AtPYL5 and AtNCED3 improved drought tolerance in Arabidopsis,30,31 and AtAREB1 was up-regulated by ABA and water stress.32 Therefore, the elevated expression levels of SoPYL5, SoNCED3, and SoAREB1 may also contribute to the improvement in drought tolerance in the present study. Leaf color is an important factor for visual appearance of leafy plants, and chlorophyll is directly correlated with the greenness of leafy vegetables.10 Additionally, vitamin C is an important nutritional component valuable for antioxidant effects.33 Therefore, chlorophyll and vitamin C content are well recognized as parameters for evaluations on the intrinsic quality of vegetables.34 Accumulating evidence has shown that water loss may inevitably affect nutritional quality of fruit and vegetables, and water loss in unfavorable conditions always gives rise to a rapid loss of vitamin C after harvest, particularly in leafy vegetables.4 Our results showed that chlorophyll and vitamin C degradation in spinach were delayed following AM1 and AMF4 treatment, and the efficacies of AM1 and AMF4

mimicking ligands capable of activating multiple ABA receptors and showing effects on preventing water loss from leaves and, thus, are promising for improving drought tolerance in agricultural crops.12,13 In addition, as AMF4 fitted more snugly into the ligand-binding pocket of the ABA-receptor proteins compared to AM1, which significantly increased the ligand−receptor binding affinity due to formation of more hydrogen bonds,13 AMF4 displayed more significant effects on water loss prevention and stomata closure. In the present study, it was found that AM1 and AMF4 markedly reduced water loss, implying their efficacies in controlling weight loss of spinach after harvest. Further studies proved that the percentage of open stomata, stomatal conductance (Gs), and transpiration rate (Tr) of spinach significantly decreased upon AM1 and AMF4 treatment. Taken together, these results indicated that AM1 and AMF4 effectively alleviated weight loss by promoting stomatal closure in spinach. Furthermore, the expression levels for the genes involved in stomatal closure (SoOST1, SoSLAC1, and SoRCAR3) significantly increased upon treatments with AM1 and AMF4. It was previously demonstrated that open stomata 1 protein kinase (OST1) and slow anion channel-associated 1 (SLAC1) were essential for stomatal closure in response to ABA.28 Overexpression of AtRCAR3 induced the maintenance of stomatal closure during Pseudomonas syringae pv tomato (Pst) DC3000 inoculation and pathogen associated molecular F


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were comparable or even better than ABA at the same concentration. Fruit and vegetables may encounter various stress conditions at the postharvest stage,35 where oxidative stress induced by reactive oxygen species (ROS) is a major reason for senescence and quality deterioration.36,37 Hydrogen peroxide and MDA contents are well received as indicators for membrane integrity and oxidative damages in response to drought and other abiotic stresses.37,38 Studies have showed that peach fruit accumulated superoxide radicals, hydrogen peroxide and MDA, which further impaired membrane permeability during postharvest ripening.38 The present study demonstrated that AM1 and AMF4 treatment alleviated the accumulation of hydrogen peroxide and MDA. Antioxidant enzymes (e.g., SOD, POD, and CAT) and nonenzymatic components (e.g., phenolic compounds, tocopherols, and carotenoids) may contribute to this process, which are responsible for balancing ROS production and scavenging.39,40 It was found that SOD and POD activities, total phenol content, and free radical scavenging activity in spinach all increased after AM1 and AMF4 application, confirming that the decrease in hydrogen peroxide may be attributed to elevated activities/contents of antioxidant enzymes and nonenzymatic antioxidants. As a consequence for the decrease in hydrogen peroxide content and the increase in antioxidative capacity, membrane lipid peroxidation after harvest may be alleviated accordingly.41 Additionally, food safety is a concern for chemical compound application in postharvest produces, in terms of AM1 and AMF4, though they are more stable than ABA; ∼30% AMF4 and ∼16% AM1 were detected in plants at 12 h after treatment,13 indicating that AM1 and AMF4 are naturally degradable or biodegradable within a relatively short period after application. In summary, ABA-mimicking ligands AM1 and AMF4 markedly up-regulated the expression of SoOST1, SoSLAC1, and SoRCAR3, promoted stomatal closure, and alleviated weight loss, which further improved drought tolerance and antioxidant capacity in spinach. Moreover, chlorophyll and vitamin C degradation were also significantly retarded. Therefore, they are effective in reducing water loss, maintaining visual quality, delaying senescence, and extending the shelf life of spinach. Further application may provide a simple and economical strategy to control water loss in vegetables and other horticultural produces.

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This work was supported by National Key Research and Development Program of China and the NSFC (31530057, 30672210). Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors sincerely thank Dr. Minjie Cao for discussion on the results and Dr. Chunyan Zhang for assistance in stomatal conductance and transpiration rate analysis.

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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/acs.jafc.8b05859. Primers for RT-qPCR analysis (Supplementary Table 1) (PDF)

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REFERENCES

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*E-mail: [email protected]. Tel.: 86-10-62836970. Fax: 86-10-82594675. ORCID

Tong Chen: 0000-0002-2456-7170 Present Address

Dr. Tong Chen, Institute of Botany, Chinese Academy of Sciences, Nanxincun 20, Xiangshan, Haidian District, Beijing 100093, China. G


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