Citrus fruits, which are cultivated worldwide, have been recognized as some of the most high-consumption fruits in terms of energy, nutrients and health supplements. What is more, a number of these fruits have been used as traditional medicinal herbs to cure diseases in several Asian countries. Numerous studies have focused on Citrus secondary metabolites as well as bioactivities and have been intended to develop new chemotherapeutic or complementary medicine in recent decades. Citrus -derived secondary metabolites, including flavonoids, alkaloids, limonoids, coumarins, carotenoids, phenolic acids and essential oils, are of vital importance to human health due to their active properties.
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Citrus fruits, which are cultivated worldwide, have been recognized as some of the most high-consumption fruits in terms of energy, nutrients and health supplements. What is more, a number of these fruits have been used as traditional medicinal herbs to cure diseases in several Asian countries.
Numerous studies have focused on Citrus secondary metabolites as well as bioactivities and have been intended to develop new chemotherapeutic or complementary medicine in recent decades. Citrus -derived secondary metabolites, including flavonoids, alkaloids, limonoids, coumarins, carotenoids, phenolic acids and essential oils, are of vital importance to human health due to their active properties. These characteristics include anti-oxidative, anti-inflammatory, anti-cancer, as well as cardiovascular protective effects, neuroprotective effects, etc.
This review summarizes the global distribution and taxonomy, numerous secondary metabolites and bioactivities of Citrus fruits to provide a reference for further study. Flavonoids as characteristic bioactive metabolites in Citrus fruits are mainly introduced.
The online version of this article doi Citrus fruits, which belong to the genus Citrus of the family Rutaceae, are of various forms and sizes from round to oblong , commonly known as oranges, mandarins, limes, lemons, grapefruits and citrons. The sensory attributes of fruits color, sweet taste, bitterness, and astringency constitute decisive organoleptic and commercial properties [ 1 ].
Citrus species are consumed mainly as fresh or raw materials for juices or are canned as segments. Additionally, Citrus fruits can also be used in the food, beverage, cosmetic and pharmaceutical industries as additives, spices, cosmetic ingredients and chemoprophylactic drugs, respectively [ 2 , 3 ]. Citrus fruits are good sources of nutrition with an ample amount of vitamin C. Besides, the fruits are abundant in other macronutrients, including sugars, dietary fiber, potassium, folate, calcium, thiamin, niacin, vitamin B6, phosphorus, magnesium, copper, riboflavin and pantothenic acid [ 4 ].
However, secondary metabolites are an especially popular topic in the present research. These constituents, also known as phytochemicals, are small molecules that are not strictly necessarily for the survival of the plants but represent pharmacological activity.
Citrus fruits contain a number of secondary metabolites, such as flavonoids, alkaloids, coumarins, limonoids, carotenoids, phenol acids and essential oils. These active secondary metabolites show several bioactivities of vital importance to human health, including anti-oxidative, anti-inflammatory, anti-cancer, as well as cardiovascular protective effects, neuroprotective effects, etc.
In addition, Citrus fruits have been used as traditional medicinal herbs in several Asian countries, such as China, Japan and Korea. Nine traditional Chinese medicines have been recorded in the Chinese Pharmacopoeia for appropriate medical use from six Citrus species [ 5 ]: C.
These peels or whole fruits mature or immature are known to treat indigestion, cough, skin inflammation, muscle pain, and ringworm infections, as well as to lower blood pressure. This review summarizes the global distribution and taxonomy, numerous secondary metabolites and bioactivities related to human health of Citrus fruits.
Especially, flavonoids as the main characteristic metabolites in Citrus fruits, which can provide benefit for human health based on their multiple bioactivities. Then, the secondary metabolites variation among different species and fruit parts were mentioned to provide a better guide for our daily use and related industries.
And China, Brazil, the U. In China, citriculture has existed traditionally, and the Citrus varieties have been naturally selected [ 7 ] see Fig. Swingle, 2 C. C itrus species are grown in countries, though production shows geographical concentration in certain areas. China is the first leading country as producers which had produced 32,, tons of C itrus fruit in Brazil is the second production country of C itrus fruits with 20,, tons in And the USA.
India, Mexico and Spain also play dominant roles in C itrus production which all produced more than 5,,00 tons in There are 14 C itrus varieties distributed in 13 provinces in China. Swingle is mainly distributed in Yunnan province; 2 C. The genus Citrus belongs to the subtribe Citrinae, tribe Citreae, subfamily Aurantioideae of the family Rutaceae. However, continual taxonomic study appears to be very complicated and controversial, mainly due to sexual compatibility between Citrus species and related genera, the high frequency of bud mutations, apomixis e.
Consequently, there has been no consensus among taxonomists as to the actual number of Citrus species. The most widely accepted taxonomic systems for Citrus are those of Swingle and Reece [ 9 ] and Tanaka [ 10 ], who recognized 16 and species, respectively.
Later, phylogenetic analysis indicated only three true species within the cultivated Citrus [ 11 ], i. In order to be convenient, the existing taxonomic systems are combined currently.
Because morphological characters are of limited use, studies have mainly focused on new taxonomy methods, i. Flavanones were used as chemotaxonomic markers to distinguish 77 Zhishi traditional Chinese medicine samples from three Citrus species [ 13 ].
Another study suggested that the content of certain monoterpenes could be as taxonomic markers between C. Plentiful active natural metabolites including flavonoids, alkaloids, coumarins, limonoids, carotenoids, phenolic acids and essential oils, have been found in Citrus fruits.
Tables in additional files have summarized these secondary metabolites isolated from peel, pulp, seed, pressed oil, juice or whole fruit from 31 common species to give a systematical profile. By these at least, the types of Citrus -derived secondary metabolites vary among different Citrus species and different fruit parts.
Moreover, flavanones, synephrine, auraptene and limonin are the most dominants among the flavonoids, alkaloids, coumarins and limonoids groups, respectively. In Additional file 1 , 48 types of flavonoids from 22 common Citrus species of different fruit parts peel, pulp, seed, pressed oil, juice or whole fruit have been summarized.
These flavonoids belong to the five classes: flavones, flavonols, flavanones, flavanonols and polymethoxylated flavones. Anthocyanins, an uncommon class of flavonoid, only appears in blood oranges of limited data in different fruit parts [ 15 ]. And flavones, flavonols and polymethoxylated flavones present in lower concentration. In addition, some of flavonoids are unique to Citrus plants.
Citrus -derived flavonoids are present in glycoside or aglycone forms, and usually do not occur naturally as aglycones but rather as glycosides, in which the aglycones are linked to a sugar moiety [ 17 ].
Among the aglycone forms, naringenin, hesperetin, apigenin, nobiletin, tangeretin and quercetin are widely detected see Additional file 1. For glycoside forms, O-glycosides, C-glycosides, rutinosides, glucosides and neohesperidosides are common. Naringin neohesperidoside , neohesperidin neohesperidoside , narirutin rutinoside , and hesperidin rutinoside are commonly present in major quantities. Sinensetin, isosinensetin, nobiletin, tangeretin, which all belong to polymethoxylated flavones, exist only as aglycones because the binding sites for sugar moieties are not occupied by hydroxyl moieties [ 18 ].
In Additional file 2 , alkaloids, coumarins, limonoids, carotenoids, phenolic acids and essential oils have also been well summarized from different Citrus species and different fruit parts.
Active alkaloids are abundant in C. Additionally, N -methyltyramine has been found at much higher concentrations than octopamine, tyramine or hordenine [ 20 ]. Coumarins are commonly found in Citrus plants high concentration in peels. Auraptene 7-geranyloxycoumarin is a major coumarin in Citrus plants. Limonoids are unique compounds occurring in the Meliaceae and Rutaceae family. Citrus a genus in the family Rutaceae limonoids are highly oxygenated triterpenoids, which are present as aglycones, glucosides, and A-ring lactones.
Also, Citrus limonoids are the metabolic precursors to limonoid aglycones and glucosides [ 21 ]. Limonin and limonin glucoside see Additional file 2 are the most abundant limonoids for the majority of Citrus species. Carotenoids are a large family of isoprenoid compounds that impart yellow, orange, and red pigments to many plants as well as the yellow-to-orange color of Citrus fruits.
Investigations have shown that the majority of phenolic acids in Citrus fruits are present in bound forms [ 23 ]. In Additional file 3 , Citrus-derived volatile compounds from 15 common Citrus Species have been summarized. These volatile compounds are mainly come from peels of Citrus fruits that have many oil chambers of unique aroma flavors, differ depending on the species and variety.
Owing to these metabolites, Citrus fruits exhibit plentiful bioactivities including anti-oxidant, anti-inflammatory, anti-cancer, anti-microbial and anti-allergy activities, as well as cardiovascular effect, neuroprotective effect, hepatoprotective effect, obesity control, etc.
Note that flavonoids especially flavanone, flavanonol and methoxylated flavones are more active compared to other secondary metabolites in Citrus for their remarkable various bioactivities.
Reactive oxygen species ROS are chemically derived from oxygen such as superoxide anion, hydroxyl radicals and hydrogen peroxide in living organisms by amount of metabolism pathways, while anti-oxidant system is able to defend against it to keep balance [ 42 ].
However, modern lifestyle involves a number of factors that may raise the level of ROS which play a critical role in the pathogenesis of various diseases such as aging, arthritis, cancer, inflammation, and heart disease, and cause oxidative stress. Citrus fruits are reported to have a good anti-oxidant ability especially because of their phenolic compounds with poly-hydroxyl groups, including phenolic acids, flavonoids and their derivatives [ 46 ].
The primary anti-oxidant mechanisms of phenolic compounds are listed below:. Direct absorption and neutralization of free radicals [ 47 ]. Enhancement of the activities of human anti-oxidant enzymes: superoxide dismutase, catalase, etc. The juices from green and ripe chinotto C.
Sun et al. Changshanhuyou, Citrus grandis L. Osbeck cv Foyou, and Citurs limon L. Different anti-oxidant assays have applied to evaluate anti-oxidant activity.
In vivo, hesperetin was administered orally and acted as a potent antioxidative agent against Cd-induced testicular toxicity in rats [ 24 ]. Hesperetin increased the glutathione and glutathione dependent enzymes in the testes of rats, by which it effectively reduced the Cd-induced oxidative stress and restored the activities of ATPases. Aranganathan and Nalini reported that hesperetin exerted an anti-lipoperoxidative effect and thereby restored the membrane-bound ATPase activity in Cd-intoxicated rat testes [ 53 ].
There were positive correlations among the results of the anti-oxidant capacities and total phenolic acids contents of the Tarhana samples [ 54 ]. The anti-oxidant potency composite index showed wide variations, ranging from Ogiwara et al. Citric acids from Citrus have been found to show anti-oxidant activity in lipopolysaccharide LPS -treated mice [ 56 ]. Korani et al. Among the phenolic acid group, gallic acid with three hydroxyl groups on the aromatic ring was the strongest anti-oxidant [ 58 ].
In contrast, the monosubstituted phenolic acids p -coumaric acid, o -coumaric acid, and 4-OH-phenylacetic acid showed very low activity. Singh et al. Choi et al. However, the bioactivity of the essential oils generally resulted from a complex interaction between its constituents, which produced both synergistic and antagonistic responses [ 62 ].
The accumulating data from studies revealed that dihydroxycoumarins were better anti-oxidants than monohydroxycoumarins and that the OH groups positioned near C6 and C7 in the coumarin skeleton played an important role in the inhibition of mushroom tyrosinase [ 63 ].
Orange C. Flavonoids, coumarin and volatile oil from Citrus fruit are showing anti-inflammatory activity, which can be used as supplement to protect against or ameliorate this chronic inflammatory diseases.
KIND OF LEMON
Effect on the clotting system of Peruvian fruit and vegetable juice. ISSN X. Objective: Verify the anticoagulant effect in vitro and in vivo of Peruvian fruit and vegetable juice and identify the coagulation pathway on which it acts. Material and Methods: Extracted juices of Ananascomosus L. Merr, Citrus limonunRisso, Carica papaya L.