Antioxidants, Vol. 12, Pages 65: Comparison of Antioxidant Properties and Metabolite Profiling of Acer pseudoplatanus Leaves of Different Colors

1. IntroductionOxidative stress disrupts the balance between reactive oxygen species (ROS), free radicals, and antioxidant defenses [1]. It can play a crucial role in the development of various diseases, such as cancer [2], malaria [3], arteriosclerosis [4], rheumatoid arthritis [5], and neurodegenerative diseases [6], and the aging process [7]. Antioxidants are synthesized in the human body or taken up from the environment through diet [8]. Although synthetic antioxidants are widely used in the food, medicine, cosmetics, and other fields, there are safety issues associated with these agents. Previous research has indicated that long-term intake of synthetic antioxidants is associated with certain teratogenic and carcinogenic risks [9].Bioactive compounds, including polyphenols, as a nutritional component, are usually presented small amounts in food, and have been reported to have various health effects, such as antioxidation, bacteriostasis, anti-inflammation, and immunity enhancement. Therefore, bioactive substances have been widely used in foods, pharmaceuticals, and cosmetics [10,11,12,13]. Polyphenols play an important role as antioxidants. Although human diets such as fruits [14], vegetables [15], tea [16], and wine [17] are rich in polyphenols, it is also necessary to find a natural, safe, and economic antioxidant in industrial production for sustainability [18]. Previous studies have found that olive rape [19], durum wheat bran [20], Fraxinus ornus bark [21], and potato peel waste [22] are good sources of natural polyphenols. In particular, maple leaves are inexpensive, easy to obtain, and have significant value for the rational use of resources and sustainable development.Anthocyanins, which are flavonoids, play an important role in physiological and biochemical processes in plants, such as leaf color change. When leaves are subjected to biotic and abiotic stresses, they are synthesized and accumulate in plant vacuoles [23,24]. In autumn, under the influence of photoperiod and low temperature, maple leaves begin to senesce, chlorophyll content begins to decline, and anthocyanin content begins to rise; therefore, maple leaves gradually change color from green to red [25]. Previous studies have shown that reactive oxygen species (ROS) levels increase and antioxidant capacity decreases during leaf senescence [26,27].Previous studies on the antioxidant capacity of maple products included analyses of maple syrup [28], maple sap [29], bark extracts [30], and leaf extracts [31]. However, to the best of our knowledge, no study has compared the antioxidant capacity and metabolite profiles of maple leaves of different colors simultaneously.

Therefore, the present study aimed to investigate the antioxidant potential of different colored maple leaves and compare the content of total polyphenols, flavonoids, tannins, chlorophyll a and b, and carotenoids in green, yellow, and red leaves. The antioxidant properties of green, yellow, and red leaves were determined using four different methods: thiobarbituric acid reactive substances (TBARS), 2,2-diphenyl-1-picrylhydrazyl radical (DPPH), metal chelation, and ferric ion-reducing antioxidant power (FRAP). Finally, to investigate the metabolic pathways associated with the colors, metabolite profiling of green, yellow, and red leaves was conducted using gas chromatography/mass spectrometry (GC/MS).

4. DiscussionPhenolic compounds with good antioxidant properties are important parameters for evaluating the antioxidant properties of plant extracts [85]. According to a previous study, the content of polyphenols in various plant leaves ranged from 11.14 to 175.35 mg/g [86]. Among the twenty four plants studied, only seven plants (including Malus domestica and Cydonia oblonga) had higher polyphenol content than red maple leaves. In this study, the antioxidant activity was measured using four different methods, and we found that the antioxidant capacity of red leaves was much higher than that of the leaves of the other two colors (red > yellow > green). The DPPH scavenging IC50 value of red leaves was 6.53 mg/mL. Herbal and low-cost biological resources have been the focus of antioxidant research. In previous research, the DPPH scavenging IC50 value of Cassia fistula L. seed extract [87], Gracilaria changii crude extract [88], and Erechtites hieraciifolius [89] was 11.07 mg/mL, 14.70 mg/mL, and 8.46 mg/mL, respectively. In addition, that of various vegetables such as Murraya koenigii, Trigonella foenum-graecum, Centella asiatica, and Amaranthus spp. was 9.62 mg/mL, 27.69 mg/mL, 19.89 mg/mL, and 27.27 mg/mL, respectively [90]. Another study showed that the IC50 values of various fruits (such as mangosteen, orange, pomelo, grapes, papaya, grape, rose apple, and jackfruit) ranged from 11.18 to 110.46 mg/mL [91]. Compared with the antioxidant properties of various biological materials, the antioxidant properties of maple leaves are not only stronger than those of low-cost biological resources but also stronger than those of some fruits. Therefore, our findings suggest that maple leaves, particularly red leaves, are a good source of polyphenols and antioxidants.Changes in leaves and carotenoids, among which the degradation of chlorophyll, is a sign of senescence [92,93]. In our observations (as shown in Figure 1), the outer leaves of maple were more converted to red sooner than the inner leaves. This may be because the outer leaves are exposed to more light and higher temperatures during the day and bear lower temperatures at night. This is consistent with previous studies showing that shading slows down the loss of chlorophyll, and the difference in temperature between day and night is conducive to the accumulation of anthocyanins [94,95]. The degradation of chlorophyll, which plays an essential role in capturing light energy, is a critical step in the accumulation of ROS during senescence. Additionally, the synthesis of anthocyanin (which acts as an antioxidant) is an important step in reducing oxidative damage [96,97]. In this study, we compared the chlorophyll content between green, yellow, and red maple leaves. The results agreed with previous reports and demonstrated that the chlorophyll content showed a decreasing tendency from green to red. In contrast, the anthocyanin and carotenoid contents were highest in the red maple leaves. These results are in agreement with a previous study that showed anthocyanin accumulation in red leaves [47]. Previous studies have reported that flavonoid/anthocyanin accumulation is affected by carotenoid accumulation [98] and chlorophyll degradation [99]. Our results also showed a positive and negative correlation between anthocyanins, and carotenoid or chlorophyll content, respectively.Phenolic compounds are important secondary metabolites in plants that mainly originate from the phenylpropane metabolic pathway [100]. In plants, photosynthetic products generate phosphoenolpyruvic acid (PEP) and erythrose 4-phosphate (E4P) through the Embden-Meyerhof-Parnas (EMP) and pentose phosphate (PPP) pathways, respectively. PEP and E4P enter the shikimic acid pathway and generate phenylalanine, the starting substrate of the phenylphenyne pathway. After a series of enzymatic reactions, flavonoids (such as catechins, proanthocyanidins, and anthocyanins) can be synthesized [100,101]. In this study, we found that the content of phenylalanine in green leaves is the highest, and that the antioxidant-related substances (such as cryptochlorogenic acid, gallic acid, neochlorogenic acid, cianidanol, α-tocopherol, and ascorbic acid) gradually increased during leaf senescence, by further metabolite analysis. These results are consistent with previous results in this study, correlating with higher total phenolic content and stronger antioxidant capacity in red leaves.In addition, previous studies have reported that the total amount of phenolic acids and antioxidant capacity were low in samples with a high content of free amino acids. The late-harvested sweet potato leaves showed higher antioxidant capacity and polyphenol content, but lower amino acid content than the early- and middle-harvests [102]. Similarly, it was found that the total flavonoid content of Ocimum basilicum L. significantly decreased under high amino acid treatment [103]. Consistent with previous studies, our study also showed that most amino acids (such as alanine, aspartic acid, leucine, phenylalanine, threonine, tyrosine, valine, glutamate, glycine, and γ-aminobutyric acid) in green leaves were present at higher levels than those in other colors. However, the polyphenolic acid content and antioxidant capacity were lower, indicating that amino acids may be converted to other phenolic compounds via the shikimic acid/phenylpropanoid/flavonoid synthetic pathway. 5. Conclusions

Maples are widely planted and are easily obtained in the northern temperate zone. In this study, we compared the polyphenol content and antioxidant properties of maple leaves of three colors (green, yellow, and red). The levels of TP, TET, TFlav, TAN, and TAC were higher in red leaves than in the other leaves. However, Chl a and b levels were lower in the red leaves. In addition, the antioxidant capacity of the red leaves was higher than that of the green and yellow leaves. PCA and HCA results revealed significant differences in metabolite profiles in maple leaves among green, yellow, and red colors. This study is the first to evaluate the level of polyphenols, antioxidant effects, and metabolites in maple leaves according to color. Therefore, red maple leaves may be used as a potential source of natural antioxidants and could be applied in the development of functional foods and pharmaceuticals.

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