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        Phytochemical constituents and biological activities of longan(Dimocarpus longan Lour.)fruit:a review

        2020-05-22 03:29:30XiaofangZhangSenGuoaChiTangHoNaishengBai

        Xiaofang Zhang,Sen Guoa,,Chi-Tang Ho,Naisheng Bai

        a College of Food Science and Technology,Northwest University,229 Taibai North Road,Xi’an,Shaanxi,710069,China

        b College of Chemical Engineering,Department of Pharmaceutical Engineering,Northwest University,229 Taibai North Road,Xi’an,Shaanxi,710069,China

        c Department of Food Science,Rutgers University,New Brunswick,NJ,08901,USA

        ABSTRACT Longan(Dimocarpus longan Lour.),as an edible fruit and traditional Chinese medicine,has been consumed for thousands of years.Longan pulp has abundant nutritional phytochemicals such as protein,carbohydrate,vitamin C,polysaccharides,polyphenols,which shows multiple biological activities including antioxidant,immunomodulatory and antitumor effects.Longan pericarp also demonstrates biological activities because of its rich content of polysaccharides and polyphenols.This review summarizes the bioactive compounds and bioactivities of longan pulp and aims to provide comprehensive information for future development of longan as a functional health food.

        Keywords:Dimocarpus longan Lour.Polysaccharides Polyphenols Flavonoids Bioactivities

        1.Introduction

        Longan (Dimocarpus longanLour.),belonging to Sapindaceae family is an important subtropical fruit tree in Southeast Asia and grown commercially in many countries,including China,Thailand,Vietnam,India,Australia,and some subtropical regions in the US [1,2].Longan has a succulent and edible aril with delicious flavor and health effects[3],which becomes more and more popular.China has been recognized as the origin of longan,where cultivation has a long history of more than 2000 years and approximately 300 cultivars have been selected for production[4].China is the largest cultivation and production nation in the world,with 73.6% cultivated area and 59.7% output [1].However,longan fruit browns rapidly at ambient temperature during storage and pericarp browning is the major problem in market[5,6].

        Longan is historically planted as an edible fruit,but can also be used for medicinal purpose [7].The health benefits of longan fruit were recorded in The Compendium of Materia Medica (Ben Cao Gang Muin Chinese) by Li Shizhen,a famous traditional Chinese medicine expert of the Ming Dynasty,who considered longan fruit as a tonic and called it the king of fruits [8].Its pulp has been used as a traditional Chinese medicine for a long time to promote blood metabolism,soothe nerves,relieve insomnia,prevent amnesia,extend longevity,cure neural pain and swelling,treat palpitation and amnesia in Asian countries [7,9-11].In addition,the plup,seed and pericarp of the fruit have been used for different disease treatments,such as improving women’s health after childbirth and increasing immunomodulatory capacity [10].Longan seed extracts also exhibit antigelatinase activity[11].Longan fruit can be consumed in many forms of products such as dried longan pulp,longan juice,longan jelly,longan wine[12]and canned longan in syrup.Nuengchamnong and Ingkaninan found that the percentage of total antioxidant activity of longan wine reached 92.6%[13].Current reports show that longan pulp possesses numerous nutritional and functional components,including carbohydrate,protein,fiber,fat,vitamin C,amino acids,minerals,polyphenols,and volatile compounds [14].Polyphenols and polysaccharides in longan pulp and pericarp contribute to antioxidant,antiglycation,antityrosinase,potent immunomodulatory and anticancer activities[15,16].Several recent studies have revealed that the extracts of longan pulp and pericarp are involved in memory enhancement[9],antianxiety[17],and reduction of serum prolactin levels in female rats[18].

        Table1 Nutritional composition per 100 g of fresh longan fruit pulpa.

        Although there are many reports on the structure and activity of polysaccharides,polyphenols and other substances in longan fruit,there is scarce comprehensive information about chemical constituents and bioactivities of longan pulp and pericarp.This review summarizes the active substances of longan pulp,such as polysaccharides,polyphenols,organic acids and volatile substances and their biological activities.We hope to provide comprehensive information for the better development of longan fruit and its effect on human health.

        2.Nutrients

        Fresh longan pulp contains carbohydrates (12%-23%),potassium K (196.5 mg/100 g),ascorbic acid (43.12-163.7 mg/100 g),and water (approximately 80%) [17].The pulp of longan fruit is the edible part which is broadly used in traditional medicine,in despite of not the part with the highest content of polysaccharides [19].Nutritional compositions of fresh longan fruit pulp are illustrated in Table1.A total of 28 different free amino acids from longan pulp has been identified including eight essential amino acids and the most abundant free amino acids are phenylalanine,alanine and glutamic acid [16].Fresh longan pulp is also rich in potassium,which maintains the normal function of human nerves and muscles.Other minerals such as iron,copper,zinc and boron are also found in longan fruit.There are 84 mg of vitamin C per 100 g of fresh longan fruit pulp which is higher than that of other common fruits.Longan aril also contains malic acid and tartaric acid[16].

        The concentration of total sugar content in longan aril increases during ripening,varying with stage of maturity and cultivar [17].The major types of sugar are sucrose,fructose and glucose [20].Sucrose was the primary accumulated form in the late growth stage of longan fruit[21].

        3.Bioactive constituents

        3.1.Polysaccharides

        Polysaccharides play an important role in living organism and widely involved in cell immune defense,cell adhesion,cell differentiation and proliferation [22].Multiple reports have found that longan pulp has different kinds of polysaccharides,so does the longan pericarp.Structural characterization of the polysaccharides has been summarized in Table2.The polysaccharides of longan fruit from Chuliang and Shixia cultivars of Guangdong province in China are the most studied.Many researchers mainly reported the structure of polysaccharides from the longan pulp,only a few polysaccharides are from longan pericarp[24].

        3.2.Polyphenols

        The antioxidant and anti-inflammatory activity of dietary polyphenols account for many health benefits of fresh fruits and vegetables[35].Polyphenolic compounds are abundant in pericarp and seeds of longan and have excellent antioxidant activity[36,37]compared to the longan pulp.The total phenolic content were in the range of 22.09-132.47 mg of gallic acid equivalents(GAE/100 g)with the average value of 75.5 mg GAE/100 g and the contribution of the free phenolic fraction to the total phenolics was 76.45%-86.93%[38].The most abundant phenolic compounds in longan pulp was 4-methylcatechol,followed by chlorogenic acid,vanillic acid,and gallic acid with an average content of 160.10,149.19,143.38,and 131.63 μg GAE/100 g,respectively,in the longan pulp of 24 representative Chinese cultivars [38].There is a literature to report that the free,bound,and total phenolic contents in non-fermented dried longan pulp were determined to be (122.56 ± 2.49),(24.40± 0.35),and (146.97 ± 2.33) mg GAE/100 g dried weight (DW),respectively,and vanillic acid,4-methylcatechol,syringic acid and gallic acid are the main polyphenols in the longan pulp[38].Other research showed that gallic acid,corilagin and ellagic acid are the major compounds in the pulp [39].In addition,longan pericarp as discarded wastes also contain a large amount of polyphenols in the range of 21.6-55.6 mg/g,in which 17 phenolic compounds has been characterized,but 18 compounds remained unidentified[36].The phenolic content and compounds in longan pericarp are summarized in Table3.

        3.3.Flavonoids

        Longan also contains some common flavonoids,a subclass of polyphenols.Total flavonoid content in longan pericarp was found slightly higher than that in longan seed and pulp [8,44].Total flavonoid content in the pulp of 24 longan cultivars ranged from 2.48 to 14.26 mg of catechin equivalents(CE)/100 g.However,only 5.9% of flavonoids were bound form in measured longan cultivars on average,which is much lower than that of litchi (26.9%)[45].The content of epicatechin ranged from 146.41-1819.57 and 17.36-166.58 μg/100 g in free and bound fractions,respectively[38],which is the most abundant single flavonoid in the pulp.Other research reports that the content of free,bound,and total flavonoids were determined to be 17.34,9.62,and 26.96 mg CE/100 g DW,respectively [16].Longan pulp also contains quercetin and isoquercitrin.Isolation of purified compounds from the extract of longan pericarp resulted in six compounds including quercetin and proanthocyanidins C1 with the content of (3.12 ± 0.76) and (9.77±0.45)mg/kg,respectively[3].Table4 lists some flavonoids found in the longan.Chemical structures of some common flavonoids and polyphenols in longan fruit are shown in Fig.1.

        3.4.Other compounds

        Longan fruit also has some organic acids and the total organic acid content in longan pulp was determined to be 20.72 mg/g DW,when fermented by lactic acid bacteria,it was significantly(P<0.05)increased to 59.62 mg/g DW [16].There are volatile components responsible for the intense aroma of the longan fruit[47,48].After analysising,Zhang et al.[49]found sixty-two different volatile compounds among which(E)-β-ocimene was the predominant terpene in longan.Esters were also important substances for longan aroma.Zhang et al.[50]has identified fifteen liposoluble compounds from longan pulp by Gas Chromatography-Mass Spectrometry(GC-MS),in which the main compositions were squalene(17.96%),hexadecanoic acid(11.22%),diisobutyl phthalate(10.78%,most likely is a contaminant),oleic acid(10.66%)and ethyl oleate(10.31%).Squalene as an attractive resource for functional food in preventingcardiovascular disease has physiological functions such as hypocholesterolemia and antioxidant[51].A literature shows that longan pulp has six cerebrosides,namely soyacerebrosides I and II,Longan cerebroside I and II,Momor-cerebroside I,and Phytolacca cerebroside[52].Longan contains alkaloids which are well-known agents for neuroprotection,anti-cancer,cardioprotection,anti-diabetics,immune stimulant,anti-inflammation and anti-viral properties[53].

        Table2 Polysaccharides from of longan pulp and pericarp.

        Table3 Polyphenol contents in longan fruit.

        Table4 Flavonoids in longan fruit.

        Fig.1.Chemical structure of flavonoids and polyphenols in longan fruit.

        4.Bioactivities

        4.1.Antioxidant activity

        Phenolic compounds have been considered to have high antioxidant ability and free radical scavenging capacity,with the mechanism of inhibiting the enzymes responsible for production of reactive oxygen species(ROS) and reduction of highly oxidized ROS[54,55].Fu et al.[45]evaluated the ferric reducing antioxidant power (FRAP) values and trolox equivalent antioxidant capacity(TEAC) values of longan,showing (8.61 ± 0.44) μmoL Fe(II)/g and(5.88±0.34)μmol Trolox/g respectively,and there is a highly positive correlation (R2= 0.8416) between the FRAP value and total phenolic content[46].The antioxidant capacity of longan in 24 cultivars has been reported and its cellular antioxidant activity(CAA)values ranged from 0.49 to 6.71 μmoL quercetin equivalents(QE)/100 g with a mean value of 2.76 μmoL QE/100 g.The CAA values suggest that phenolics and flavonoids are the main contributors to the antioxidant capacity of longan fruit[38].The FRAP value of longan seed also was higher than that of peel and pulp[56],with pulp being the lowest.

        4.2.Immunomodulatory

        Polysaccharides from many natural sources have been reported to have immunomodulating function[57].LPD2,an active polysaccharide from longan pulp,showed strong effect on activation of macrophages phagocytosis,as well as on proliferation of splenic lymphocytesviathe toll-like receptor 2 (TLR2) and 4 (TLR4)mediated myeloid differentiation factor 88/interleukin receptor associated kinases 4-tumor necrosis factor receptor associated factor 6 (MyD88/IRAK4-TRAF6) signaling pathway [10,21,25,28].Higher molecular weight,the acetyl groups and (1→4)-β-Glc are the main reasons for stronger immunomodulatory of LPD2.Preliminary testsin vitroshowed a water-soluble polysaccharide fraction(LP1)and its sulfate derivative(LP1-S)could stimulate murine lymphocytes proliferation and increase pinocytic activity of murine macrophages and production of nitric oxide(NO),interleukin 6(IL-6),interleukin(IL-1β)and tumor necrosis factor-alpha(TNF-α)in macrophages[29].Two derivatives of longan pulp polysaccharide(LPI)after alkali treatment,LPI1 or LPI2,could significantly enhance splenocyte proliferation and natural killer (NK) cell cytotoxicity due to the presence of slightly dissociated sphere-like conformation or single-helix chain,resulting from an investigation of the relationship between molecular conformation and immunomodulatory activity [58].Polysaccharides in aqueous solution exhibit various conformations,such as sphere-like,random coil,semiflexible chain,stiff chain,helical chain including single-helix and triple-helix [59,60].Longan could provide potential dietary supplement for the treatment of inflammatory-related diseases[61].

        4.3.Anticancer activity

        A pure polysaccharide (LPS1) from longan pulp has positive effect against hepatoma cells with dose-dependent manner probably because of immunomodulatory behavior of(1→6)-α-D-glucan,but had negative effect against breast cancer cells [27].The anticancer activity of (1→3)-β-D-glucan and (1→6)-β-D-glucan has been confirmed [62].A new water-soluble polysaccharide from longan pulp(LP1)had significantly high antitumor activity against SKOV3 and HO8910 tumor cellsin vitroexperiments,with inhibition percentages of 40% in the concentration of 40 mg/L and 50% in the concentration of 320 mg/L,respectively [28].Four purified longan polysaccharides (LP I-IV) and crude longan pulp polysaccharides have an inhibitory effect on A549,HeLa and HepG2 cell proliferation,respectively,ranged 5.6%-16.8%,8.3%-23.2%and 4.7%-29.5%,and LP III showed stronger inhibition on A549 and HepG2 cells than the crude longan pulp polysaccharides[63].The contributions of the factors related to the anti-tumor activity of polysaccharide were of the order of water solubility >chain conformation >the weight-average molar masses(Mw)[64].

        4.4.Anti-tyrosinase activity

        Anti-tyrosinase activity is mainly associated with the longan pericarp extract.The longan pericarp extract from ultra-highpressure-assisted extraction of 500 MPa showed the highest percentage of anti-tyrosinase activity (23.6 ± 1.2) at a concentration of 100 g/mL,when compared to conventional extractions(19.5±0.6)[65].Some tyrosinase inhibitors act through hydroxyl groups that bind with the active site on tyrosinase resulting in steric hindrance or changed conformation[66].The ultrasonic treatment of polysaccharides from longan fruit pericarp(PLFP)increased the inhibition of tyrosinase activity in a non-competitive manner[67],which was in agreement with the report by Rout and Banerjee[68].Both fresh and dried longan seed clearly showed tyrosinase inhibitory activity in a concentration-dependent manner and the half maximal inhibitory concentration (IC50) values for fresh and dried seed extracts were 2.9 and 3.2 mg/mL,respectively[69].

        The tyrosinase inhibiting activity of longan polyphenols has been studied.Guan et al.[70]reported that the inhibition rate of longan polyphenol extract on tyrosinase activity was dosedependent and the inhibition rate increased with increasing sample concentration.The inhibitory activity may be due to the presence of ellagic acid,gallic acid,corilagin and ethyl gallate.These polyphenols contain many phenolic hydroxyl groups,which are similar in structure to the substrate and can bind copper ion active center of tyrosinase,eliminate active oxygen and antagonize tyrosinase activation.Inhibition kinetics studies confirmed that longan polyphenols reversibly and competitively inhibit tyrosine diphenolase.That is,the combination of longan polyphenols and substrates with enzymes compete with each other,and the spatial structure of enzyme has not changed irreversibly.Longan polyphenols are competitively combined with the copper ion active center of tyrosinase reducing the concentration of tyrosinase in the reaction system,thereby inhibiting the synthesis of pigment substances.Kubo et al.[71]also reported the corresponding mechanism of tyrosinase inhibitory activity,they found that quercetin can reduce tyrosinase activity by binding to tyrosinase active centers.

        4.5.Anti-osteoporotic activity

        Longan fruit extract(LFE)inhibits osteoclast differentiation evidenced by repressing mRNA expression of osteoclast marker and reducing the number of tartrate resistant acid phosphatase(TRAP)-positive multinucleated cells in RAW264.7 cells.[72].Previous study demonstrated that LFE induces osteoblast differentiationviathe phosphorylation of extracellular signal-regulated kinase1/2(Erk1/2)-dependent runt-related transcription factor 2 (RUNX2)activation [73].Other report shows that longan pulp polysaccharides could effectively promote chondrocytes growth and enhance secretion and synthesis of cartilage extracellular matrix by upregulating expression levels of aggrecan,collagen II and sox9[74].

        4.6.Prebiotic activity

        Longan pulp polysaccharides exhibited stronger stimulation than LP-H (longan pulp polysaccharide were extracted with hot water)and LP-S(longan pulp polysaccharide were extracted with superfine grinding)on the proliferation ofLactobacillus plantarum,

        Lactobacillus bulgaricus,Lactobacillus fermentumandLeuconostoc mesenteroides,but it is inferior to fructooligosaccharide effect on bacteria mentioned above proliferation [2].Longan hydrolysate with a 21%degree of hydrolysis showed a higher prebiotic value and bacterial growth level forLactobacillus acidophilusandBifidobacterium lactisthan that previously reported for the enzymatically extracted mangosteen aril[75,76].

        4.7.Other activities

        The acetylcholinesterase inhibitory activity of longan pulp polysaccharides(25.40%)was higher than that ofFlammulina velutipespolysaccharides (18.51%) [77,78].Polysaccharides of longan fruit pericarp showed a good and stable anti-glycation activity[31].Polyphenol-enriched longan pericarp extracts show antihyperglycaemic activity in bothin vitroandin vivostudies[40].Longan pericarp proanthocyanidins has α-amylase inhibitory activity with IC50of 0.075 mg/mL for uncompetitive α-amylase inhibition [79].In addition,longan seed extract shows antimicrobial,antifungal,and anticancer activities[80-82].

        5.Conclusion

        Longan fruit has gained much attention in recent years.Polyphenols and polysaccharides of longan pulp have been confirmed to have many bioactivities such as antioxidant,immunomodulatory,anticancer,anti-osteoporotic,prebiotic,memory-enhancing,and anxiolytic effects.Longan pericarp has abundant polyphenols,flavonoids and polysaccharides compared to longan pulp,which show antioxidant,anti-tyrosinase,anti-hyperglycaemic activities.We hope this review will provide comprehensive information to both academic research and nutritional product development of longan and its byproducts during processing.

        Declaration of Competing Interest

        The authors declare no competing interest.

        Acknowledgement

        This project was supported by the National Natural Science Foundation of China(No.31570348).

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