You are on page 1of 10

International Journal of Food Sciences and Nutrition

ISSN: 0963-7486 (Print) 1465-3478 (Online) Journal homepage: http://www.tandfonline.com/loi/iijf20

Phenolic compositions and antioxidant activities


of grapefruit (Citrus paradisi Macfadyen) varieties
cultivated in China

Wanpeng Xi, Guiwei Zhang, Dong Jiang & Zhiqin Zhou

To cite this article: Wanpeng Xi, Guiwei Zhang, Dong Jiang & Zhiqin Zhou (2015): Phenolic
compositions and antioxidant activities of grapefruit (Citrus paradisi Macfadyen)
varieties cultivated in China, International Journal of Food Sciences and Nutrition, DOI:
10.3109/09637486.2015.1095864

To link to this article: http://dx.doi.org/10.3109/09637486.2015.1095864

View supplementary material

Published online: 12 Oct 2015.

Submit your article to this journal

View related articles

View Crossmark data

Full Terms & Conditions of access and use can be found at


http://www.tandfonline.com/action/journalInformation?journalCode=iijf20

Download by: [University of Waterloo] Date: 15 October 2015, At: 07:05


http://informahealthcare.com/ijf
ISSN: 0963-7486 (print), 1465-3478 (electronic)

Int J Food Sci Nutr, Early Online: 1–9


! 2015 Taylor & Francis. DOI: 10.3109/09637486.2015.1095864

RESEARCH ARTICLE

Phenolic compositions and antioxidant activities of grapefruit (Citrus


paradisi Macfadyen) varieties cultivated in China
Wanpeng Xi1,3, Guiwei Zhang1, Dong Jiang3, and Zhiqin Zhou1,2
1
College of Horticulture and Landscape Architecture, Southwest University, Chongqing, China, 2Key Laboratory of Horticulture Science for Southern
Mountainous Regions, Ministry of Education, Chongqing, China, and 3Citrus Research Institute, Chinese Academy of Agricultural Sciences,
Chongqing, China
Downloaded by [University of Waterloo] at 07:05 15 October 2015

Abstract Keywords
The phenolic compounds in different fruit parts including the flavedos, albedos, segment Antioxidant capacity, flavonoid, grapefruit,
membranes, juice vesicles and seeds of nine grapefruit varieties cultivated in China were phenolic acid, pummelo
determined and their antioxidant capacities were evaluated using three methods. Naringin and
neohesperedin were the dominant flavonoids in all grapefruit tested. Fenghongtangmuxun History
and Jiwei flavedo had the highest contents of naringin (5666.82 mg/g DW) and neohesperedin
(1022 mg/g DW), respectively. Gallic acid was the major phenolic acid in all grapefruit tested, Received 27 May 2015
and Jiwei juice vesicles had the highest content of gallic acid (343.7 mg/g DW). Revised 4 August 2015
Fenghongtangmuxun juice vesicles were rich in chlorogenic acid (110.23 mg/g DW), caffeic Accepted 15 September 2015
acid (53.86 mg/g DW) and ferulic acid (23.12 mg/g DW). Overall, the flavedo was rich in flavonoid, Published online 13 October 2015
while juice vesicle had high amounts of phenolic acid. The Jiwei, Fenghongtangmuxun, Maxu,
Huoyan and Hongmaxu grapefruit cultivars contained more phenolics and exhibited higher
antioxidant capacities than Shatianyou and Liangpingyou pummelos, and were good sources
of natural phytochemical antioxidants.

Introduction
there is much evidence that grapefruit have strong antioxidant,
Polyphenols are one of the most important group of phytochem- anti-microbial and anti-inflammatory properties. Therefore,
ical antioxidants in fruits, and there is increasing attention and grapefruit are becoming an increasingly popular health-promoting
interest in these compounds due to their powerful protection fruit. In the current literature, different grapefruit genotypes have
against many chronic diseases including cardiovascular disease been described, such as Redblush (Njoroge et al., 2005), Marsh,
(Yamada et al., 2011), diabetes (Oboh & Ademosun, 2011) and Redblush, Star Ruby (Chaudhary et al., 2012), Duncan (Zhao
cancer (Du & Chen, 2010). As an important global fruit crop, et al., 2013), Ruby red and Marsh seedless (Folimonova et al.,
citrus fruits are abundant in polyphenols, primarily involving 2009). However, previous studies have primarily focused on the
flavonoids and phenolics acids (Peterson et al., 2006). Some volatile constituents (Njoroge et al., 2005), evaluating the
researchers have identified and quantified phenolic compounds bioactivities of citrus essential oils (Choi et al., 2000; Zhang
and analyzed the antioxidant capacities of citrus fruits such as et al., 2011a), determining the origin of grapefruit (Jing et al.,
limes, grapefruit, sweet oranges, lemons, tangerines (Abad-Garcia 2015), Huanglongbing (citrus greening) resistance (Folimonova
et al., 2012; Goulas & Manganaris, 2012; Kelebek et al., 2008), et al., 2009; Zhao et al., 2013), and limonoid metabolism. To date,
sour orange (Tripoli et al., 2007), mandarin fruit (Zhang et al., the information on grapefruit cultivated in China has been scarce,
2014) and pummelos (Xi et al., 2014). However, only a few though we recently investigated the flavonoid compounds and
studies have determined the polyphenols compounds and antioxi- antioxidant activity of Chinese local pummelo.
dant capacities of grapefruit varieties cultivated in China, The objective of the present study was to determine the content
especially in the different parts of the fruit. and composition of phenolic compounds in five different fruit
Grapefruit (Citrus paradisi Macfadyen) is a group of large parts, flavedos, albedos, segment membranes, juice vesicles and
citrus of recent origin, likely resulting from a cross between seeds, of nine grapefruit varieties cultivated in China and to
pummelo and sweet orange (de Moraes et al., 2007), and it is evaluate their antioxidant capacities. The results obtained were
widely cultivated in the tropical and some subtropical provinces compared with two control Shatianyou and Liangpingyou pum-
of China. Grapefruit is an excellent source of many nutrients and melos, to provide information for the future utilization of Citrus
phytochemicals that contribute to a healthy diet, mainly including germplasm.
polyphenols, vitamin C, lycopene, pectin and fibre. Currently,
Materials and methods
Chemicals
Corresponding: Zhiqin Zhou, College of Horticulture and Landscape
Architecture, Southwest University, Chongqing, China. Tel: +86 23 Eriocitrin, naringin, hesperidin, naringenin, hesperetin, rutin,
68250229. Fax: +86 23 68251274. E-mail: zqzhou2013@swu.edu.cn diosmin, eriodictyol, sinensetin, nobiletin, tangeretin, gallic acid,
2 W. Xi et al. Int J Food Sci Nutr, Early Online: 1–9

Table 1. Grapefruit and pummelo varieties used in the present study.

Number Repository number ScientiEc name Chinese name Abbreviation


1 LG0120 Citrus paradisi Mac. Aolangbulangke AL
2 LG0245 Citrus paradisi Mac. Jiwei JW
3 LG0094 Citrus paradisi Mac. Fenghongtangmuxun FH
4 LG0096 Citrus paradisi Mac. Xinglubi XL
5 LG0093 Citrus paradisi Mac. Maxu MX
6 LG0114 Citrus paradisi Mac. Huoyan HY
7 LG0248 Citrus paradisi Mac. Ruihong RH
8 LG0115 Citrus paradisi Mac. Sibeitimaxu SM
9 LG0243 Citrus paradisi Mac. Hongmaxu HM
10 LG0004 Citrus grandis (L.) Osbeck Shatianyou ST
11 LG0006 Citrus grandis (L.) Osbeck Liangpingyou LP

chlorogenic acid, caffeic acid and ferulic acid were obtained from 330 nm, chlorogenic acid, caffeic acid and ferulic acid were
Sigma (St. Louis, MO). 2,2-diphenyl-1-picrylhydrazyl radicals detected at 320 nm (Supplementary Figure S1). All compounds
(DPPH), 2,4,6-tris (2-pyridyl)-S-triazine (TPTZ), dimethyl sulph- were identified by comparing their retention time and the spectral
oxide (DMSO), acetic acid and acetonitrile were purchased from characteristics of peaks with those of standards and were
Fluka (St. Louis, MO). All other reagents were of analytical grade quantified based on the peak area of the sample and the
Downloaded by [University of Waterloo] at 07:05 15 October 2015

and were obtained from Sinopharm Chemical Reagent Co., Ltd. corresponding standard.
(Shanghai, China).
Antioxidant activity assays
Fruit materials
The antioxidant activity assays were performed using the 2,2-
Nine grapefruit (C. paradisi Macf.) and two pummelo (C. grandis diphenyl-1-picrylhydrazyl radicals (DPPH), 2,20 -azino-bis
Osbeck.) varieties were grown at the National Citrus Germplasm (3-ethylbenzthiozoline-6)-sulphonic acid (ABTS) and ferric
Repository, Citrus Research Institute of Chinese Academy of reducing/antioxidant power (FRAP) methods. The DPPH assay
Agricultural Sciences, Chongqing, China (Table 1). Fruits were was conducted according to the method described by Barreca
harvested at the commercial maturity stage based on external et al. (2011). Each sample (50 mL) was mixed with 63 mM of
color and size uniformity (Figure 1). After harvest, grapefruit and DPPH in methanol to a Enal volume of 4.0 mL. After 25 min, the
pummelo fruits were divided into flavedo, albedo, segment absorbance was detected at wavelength of 517 nm. The inhibition
membrane, juice vesicle and seed. All fruit parts were sliced into percentage of the radical scavenging activity was the DPPH value.
small cubes, frozen using liquid nitrogen and stored at –80  C ABTS values were obtained according to the method described by
until analysis. Barreca et al. (2010). A total of 5 mL aqueous ABTS solution
(7 mM) was added to 88 mL of a 140 mM of potassium per sulfate
Extraction of phenolic compounds solution. The mixture was stored in dark at 29  C for 14 h before
use. The decrease in absorbance was measured over 6 min at
First the cubes were lyophilized, ground, and sieved through a 40-
734 nm. The FRAP assay was determined following the method of
mesh sieve. Extraction was carried out according to the method of
Jang et al. (2010). A 20 mL aliquot of the fruit extract was mixed
Ramful et al. (2011) with light modifications. Lyophilized powder
with 1.8 mL of FRAP reagent and 1.8 mL of deionized water.
samples (1 g) were homogenized with methanol (80%, 12 mL) and
After 30 min, the absorbance was detected at a wavelength of
dimethyl sulphoxide (1:1, v/v). The mixture was shaken for 12 h
593 nm. Aqueous solutions of 0–5 mM ferrous sulphate heptahy-
and then centrifuged at 3000 g for 10 min at 4  C. Methanol
drate were used for calibration, and the reducing power was
(80%, 24 mL) was added to the residue and the same procedure
expressed in mM. All absorbance values were determined using
was repeated. Supernatants from both extractions were collected
the above mentioned spectrophotometer. All tests were run in
and diluted to 50 mL with methanol. The solutions were then
triplicate.
stored at –20  C for the determination of individual flavonoids,
phenolic acids and antioxidant activity.
Statistical analysis
Individual phenolic compound determination All data are expressed as the means ± standard deviation of three
replicates. Statistical analysis was performed using SPSS v19.0
The individual phenolic compounds were determined by HPLC
software (SPSS Inc., Chicago, IL). Significant differences among
method as described in our previous report (Zhang et al., 2011b).
the samples were calculated using one-way ANOVA followed by
After filtration on Millipore membrane (0.22 mm), the solution
Duncan’s multiple-range test at the 5% level (p  0.05).
(10 mL) was injected into the HPLC system. Chromatographic
separation was carried out on a reversed-phase column (ZORABX
SB-C18, 250 mm  4.6 mm internal diameter). The mobile phase Results and discussion
was composed of (A) 0.1% formic acid (aqueous) and (B)
Individual phenolic compound contents
methanol. Gradient elution was performed as follows: from
0–20 min, 37–50% B; from 20–35 min, 50–80% B; In the present study, a total of 15 phenolic compounds, including
from 35–40 min, 80–100% B; from 40–50 min, 100% B; and eight flavanones, three polymethoxylated flavones (PMFs) and
from 50–60 min, 37–50% B. The column temperature was four phenolic acids compounds, were identified in the flavedo,
maintained at 25  C, and the flow rate was 0.7 mL/min. albedo, segment membrane, juice vesicle and seed of the
Eriocitrin, naringin, hesperidin, naringenin, hesperetin, rutin, grapefruit and pummelos tested (Table 2). We found that the
diosmin, eriodictyol, and gallic acid were detected at wavelengths similar variation patterns of the polyphenols components and
of 283 nm, sinensetin, nobiletin and tangeretin were detected at contents were observed in the different varieties studied
DOI: 10.3109/09637486.2015.1095864 Phenolic compositions and antioxidant activities of grapefruit 3

Figure 1. Grapefruit and pummelo varieties used in the present study. a–k indicated the Aolangbulangke, Jiwei, Fenghongtangmuxun, Xinglubi, Maxu,
Huoyan, Ruihong, Sibeitimaxu, Hongmaxu, Shatianyou and Liangpingyou, respectively.

(Figure 2), which is similar to the recent result obtained by our Xinglubi juice vesicle had the highest naringenin content. The
group for wild mandarin fruit (Zhang et al., 2014). The conclusion content of narirutin ranged from nd to 25.96 mg/g DW, with Jiwei
Downloaded by [University of Waterloo] at 07:05 15 October 2015

that flavonoids are genetically controlled was further confirmed flavedo containing the highest amount. Narirutin was not detected
by the present result. in albedo, juice vesicle or seed. The diosmin and hesperetin
contents varied from nd to 49.06 mg/g DW and nd to 16.76 mg/g
DW, respectively. Fenghongtangmuxun flavedo had the highest
Flavanones contents
diosmin and hesperetin contents, which were detected only in its
Flavanones were the major flavonoid in the grapefruits tested, and flavedo, segment membrane and juice vesicle.
naringin was the predominant flavanone, followed by neohesper- Flavanones are the typical polyphenols of Citrus species (Khan
idin. The naringin contents varied from 1731.3 to 5666.8 mg/g et al., 2014). Previous study showed that hesperidin, didymin and
DW in flavedos, from 50.18 to 366.3 mg/g DW in albedos, from narirutin are the characteristic flavanones of sweet orange,
901.0 to 3787.3 mg/g DW in segment membranes, from 482.4 to tangelo, lemon and lime (Ooghe et al., 1994), while hesperidin
2699.0 mg/g in juice vesicles, and from 52.93 to 359.5 mg/g DW in was the dominant flavanone in mandarin fruit (Zhang et al.,
seeds. Fenghongtangmuxun flavedo had the highest naringin 2014). Naringenin is rich in sour orange. Our previous study
content. Much higher levels of naringin were detected in showed that naringin was the predominant flavanone in pummelo
Aolangbulangke, Fenghongtangmuxun, Xinglubi, Huoyan, varieties, whereas naringin and neohesperidin were the principal
Ruihong and Hongmaxu grapefruit than in the two control flavanones in grapefruit (Xi et al., 2014), which was further
Shatianyou and Liangpingyou pummelos. The naringin content of confirmed by the present results. Cano et al. (2008) found that the
all tested grapefruit flavedos, segment membranes and naringin contents of mandarin fruit varieties varied from 2.6 to
juice vesicles were 1.95–3.58 times, 2.49–7.30 times, 1.66–4.99 34.4 mg/100 g DW, whereas orange varieties had contents ranging
times and 1.58–5.60 higher, respectively, than those of the from 8.8 to 28.7 mg/100 g DW. Our previous study showed that
control Shatianyou and Liangpingyou pummelos. Higher naringin levels ranged from 734.61 to 9788.58 mg/g DW in 28
levels of naringin were also found in Aolangbulangke, Chinese local pummelo varieties and four grapefruit, and the
Fenghongtangmuxun, Huoyan and Hongmaxu seeds than in the contents in grapefruit were 1–3.98 times higher than those in
control Shatianyou and Liangpingyou pummelos. pummelo. In the present study, we found that the naringin levels
The neohesperidin contents varied from 23.07 to 1022 mg/g in grapefruits ranged from 50.18 to 5666.82 mg/g DW, and the
DW in flavedos, from 5.64 to 280.3 mg/g DW in albedos, from concentrations were 1.58-5.60 times higher than those in the local
16.34 to 565.2 mg/g DW in segment membranes, from 11.09 to pummelos varieties, which further prove that grapefruits have
356.9 mg/g in juice vesicles, and from 3.33 to 189.2 mg/g DW in significantly greater naringin contents than pummelos. On the
seeds. Jiwei had the highest neohesperidin content. Much higher contrary, Girennavar et al. (2008) found that pummelo had 1.5 to
levels of neohesperidin were detected in all grapefruit tested than 2.3 times more naringin than seven hybrid grapefruits, which
them in the control Shatianyou and Liangpingyou pummelos. The could be due to a difference in varieties.
neohesperidin contents of the grapefruit tested were higher than In this study, we found that the neohesperidin contents of the
that in the corresponding tissues in the control Shatianyou and grapeftuit varieties tested ranged from 19.39 to 1022 mg/g DW,
Liangpingyou pummelos by 4.21 to 44.29 times in flavedos, 4.43 whereas the neohesperidin contents of 14 wild mandarin fruit
to 49.7 times in albedos, 3.75 to 28.51 times in segment ranged from nd to 11.69 mg/g DW (Zhang et al., 2014). In
membranes, 4.24 to 27.69 times juice vesicles and 3.35 to 56.75 addition, we found that the hesperidin contents of the grapeftuit
times DW in seeds. varieties tested ranged nd to 246.05 mg/g DW, but almost no
Eriocitrin was detected in almost all of the grapefruit varieties hesperidin was detected in the control Shatianyou and
tested, varying from nd (not detectable) to 125.39 mg/g DW. Jiwei Liangpingyou pummelos, which was consistent with another
flavedo had the highest level of eriocitrin, and Jiwei albedo, recent study (Xi et al., 2014). Cano et al. (2008) reported
segment membrane and juice vesicle were also rich in eriocitrin hesperidin contents of 13.2–60.6 mg/100 g DW and 48.1–
(448.59 mg/g DW). The hesperidin content varied from nd to 104.7 mg/100 g DW in mandarin and orange pulp, respectively.
246.05 mg/g DW in all grapefruit tested. Maxu segment membrane The hesperidin content of lemon was 1.25 g/100 g DW in peel and
presented the highest level of hesperidin content, and Maxu juice 0.28 g/100 g DW in pulp, respectively (Del Rı́o et al., 2004). In the
vesicle was also rich in hesperidin (119.8 mg/g DW). The present study, the content of narirutin in the grapefruit varieties
naringenin content ranged from nd to 33.29 mg/g DW, and tested ranged from nd to 25.96 mg/g DW, while Cano et al. (2008)
Downloaded by [University of Waterloo] at 07:05 15 October 2015
4
W. Xi et al.

Table 2. Phenolic composition and concentrations (mg/g DW) in different parts of nine grapefruit and two pummelo varieties.

Flavanones Polymethoxylated Favones Phenolics acid

Varieties Eriocitrin Naringin Hesperidin Naringenin Narirutin Neohesperedinn Diosmin Hesperetin Sinensetin Nobiletin Tangeretin Gallic acid Chlorogenic acid Caffeic acid Ferulic acid

Flavedo
AL 7.00 ± 0.54fg 2325.2 ± 269.3d nd 10.64 ± 1.36d 23.74 ± 3.30a 60.82 ± 6.28c 12.2 ± 1.36d 3.89 ± 0.42c 2.31 ± 0.36c 6.53 ± 0.85g 15.01 ± 1.06e 38.8 ± 4.32g 15.77 ± 1.06h 3.65 ± 0.24b 0.45 ± 0.08e
JW 125.4 ± 11.4a 5380.3 ± 182.3b 49.59 ± 2.86b 12.98 ± 0.98c 25.96 ± 2.62a 1022 ± 97.63a 19.5 ± 2.05c 0.57 ± 0.09d 1.03 ± 0.19d 14.96 ± 1.23ef 41.55 ± 0.32a 130.9 ± 9.63a 33.57 ± 2.69g 0.43 ± 0.07d 1.12 ± 0.11cd
FH 32.52 ± 2.54b 5662.1 ± 401.3a 50.38 ± 3.25b 14.6 ± 1.12b 16.14 ± 1.74b 165.3 ± 7.65b 49.1 ± 5.36a 16.76 ± 1.18a 3.94 ± 0.25b 13.17 ± 0.96f 15.9 ± 0.64e 52.16 ± 4.35e 50.83 ± 3.33e 0.59 ± 0.11d 0.81 ± 0.05d
XL 16.63 ± 2.31d 1906.3 ± 233.4d 22.03 ± 1.98f 2.56 ± 2.26c 18.94 ± 0.96b 47.21 ± 16.4f 9.4 ± 0.85e 4.49 ± 0.39c 5.31 ± 0.32a 7.77 ± 1.54d 6.81 ± 1.03de 37.82 ± 3.21g 24.64 ± 8.26c 0.74 ± 0.23cd 1.31 ± 0.20c
MX 20.76 ± 1.21f 4775.1 ± 368.7d 46.9 ± 5.22bd nd 3.18 ± 0.27f 126.8 ± 18.65e 29.7 ± 3.34b 10.6 ± 1.06b 4.67 ± 0.31ab 21.81 ± 1.89b 25.97 ± 3.22b 42.55 ± 2.78f 53.58 ± 3.17d nd 0.73 ± 0.06d
HY 26.69 ± 1.55e 5640.7 ± 196.5a 61.97 ± 3.67a 10.07 ± 1.54d 17.43 ± 1.09b 138.3 ± 9.63d 31.8 ± 2.98b 9.28 ± 0.83b 5.19 ± 0.47a 17.86 ± 1.36d 18.77 ± 1.56d 58.63 ± 3.69c 79.65 ± 5.32b 3.36 ± 0.45b 2.44 ± 0.32b
RH 15.25 ± 3.36d 2056.4 ± 387.3e 21.66 ± 2.02f 4.94 ± 3.26e 10.11 ± 0.56cd 37.49 ± 8.24f 2.33 ± 0.32h 3.46 ± 0.45c 3.98 ± 0.29b 9.91 ± 2.01c 21.14 ± 1.18c 55.68 ± 6.34d 31.63 ± 5.11f nd 0.36 ± 0.09e
SM 16.95 ± 1.97d 2138.6 ± 285.5e 15.43 ± 3.18e 0.51 ± 0.08f 1.78 ± 0.24f 59.8 ± 6.98de 4.36 ± 0.75f 3.54 ± 0.29c 1.82 ± 0.23c 5.85 ± 1.23e 10.07 ± 1.59cd 46.99 ± 3.63a 23.05 ± 4.52f 1.11 ± 0.21c nd
HM 20.91 ± 1.65d 5666.8 ± 354.1a nd 16.35 ± 1.69a 13.08 ± 12.4c 117.82 ± 6.34f 8.63 ± 1.12ef 5.18 ± 0.38c 3.93 ± 0.46b 24.58 ± 1.75a 10.82 ± 1.36f 71.71 ± 8.29b 86.34 ± 7.69a 3.88 ± 0.45b nd
ST 18.84 ± 2.03d 1731.3 ± 96.2f nd 0.94 ± 0.12f 7.57 ± 0.85e 27.93 ± 0.56g nd nd 3.87 ± 0.29b nd 5.63 ± 0.74g 39.35 ± 4.41g 15.96 ± 1.04h nd 1.18 ± 0.16c
LP 17.42 ± 3.22d 1581.6 ± 107.0f nd 5.11 ± 0.81e 12.01 ± 1.69c 23.07 ± 1.56g 4.38 ± 0.56g 4.78 ± 0.54c nd 3.32 ± 0.44h 7.09 ± 0.54g 26.19 ± 3.26h 32.39 ± 4.58g 17.74 ± 2.03a 3.26 ± 0.45a
Albedo
AL 12.26 ± 2.67c 109.9 ± 13.68e nd 1.45 ± 0.10e 0.93 ± 0.06a 39.39 ± 6.38f nd nd nd nd nd 18.69 ± 2.69bc nd 1.37 ± 0.21a 5.24 ± 0.69a
JW 48.59 ± 3.82a 223.2 ± 17.55f 13.46 ± 1.65b 5.65 ± 0.32ab nd 280.3 ± 21.2a nd nd nd nd nd 37.6 ± 4.35c 3.62 ± 0.26d 0.32 ± 0.08d nd
FH 45.71 ± 5.11b 259.3 ± 17.36d nd 4.31 ± 0.29c nd 46.36 ± 6.96d nd nd nd nd nd 36.59 ± 1.98c 5.263 ± 0.56c 0.61 ± 0.06b nd
XL 9.96 ± 2.09e 123.3 ± 45.61b 7.29 ± 0.58d 1.81 ± 0.44a nd 10.86 ± 5.34f nd nd nd nd nd 16.51 ± 3.26ab nd 0.63 ± 0.09b nd
MX 23.36 ± 1.55d 283.3 ± 24.66c 11.1 ± 0.84c 5.17 ± 0.31bc nd 56.98 ± 3.69c nd nd nd nd nd 40.62 ± 5.14a nd 0.49 ± 0.08c nd
HY 31.26 ± 2.68c 366.3 ± 19.56a 24.33 ± 1.35a 3.99 ± 0.27c nd 43.66 ± 9.85e nd nd nd nd nd 31.81 ± 0.24d nd nd nd
RH 9.77 ± 1.54e 124.5 ± 21.54b 9.59 ± 0.64c 1.63 ± 0.17cd nd 16.39 ± 6.31b nd nd nd nd nd 16.02 ± 0.26c nd 0.53 ± 0.08bc nd
SM 5.72 ± 0.95f 88.6 ± 15.55h 4.89 ± 0.29e 6.38 ± 0.72a nd 7.05 ± 8.23c nd nd nd nd nd 11.16 ± 1.01a nd 0.31 ± 0.07d nd
HM 8.83 ± 0.94fg 205.8 ± 17.37g 4.72 ± 0.37e 3.13 ± 0.39d nd 47.86 ± 5.51d nd nd nd nd nd 41.83 ± 2.19a nd 1.68 ± 0.15a nd
ST 7.22 ± 0.53g 50.18 ± 3.26j nd nd nd 8.89 ± 2.16g nd nd nd nd nd 19.28 ± 1.93e 70.87 ± 5.16a 0.32 ± 0.06d nd
LP 2.55 ± 0.38h 68.62 ± 9.83i nd 1.27 ± 0.09e nd 5.64 ± 0.07h nd nd nd nd nd 13.85 ± 0.07f 32.57 ± 4.41b nd nd
Segment membrane
AL nd 1527.9 ± 93.82f nd 2.59 ± 0.45b 0.93 ± 0.08a 27.21 ± 2.36e 3.12 ± 0.41b 0.75 ± 0.05b nd 1.68 ± 0.26a 2.38 ± 0.34a 15.35 ± 3.22d nd nd 2.67 ± 0.19a
JW 105.25 ± 8.33a 2894.1 ± 36.89h 70.40 ± 5.64b 1.81 ± 0.21cd nd 565.2 ± 85.34a 1.38 ± 0.12d 2.21 ± 0.16b 1.25 ± 0.16a 4.97 ± 0.13b 11.29 ± 0.23a 64.92 ± 4.97b nd nd 1.96 ± 0.23a
FH 11.64 ± 1.36d 2944.6 ± 103.2d nd 10.35 ± 1.32ab 0.89 ± 0.11a 126.0 ± 9.63b 6.48 ± 0.56a 2.13 ± 0.22b nd 1.41 ± 0.15b 2.23 ± 0.19b 55.54 ± 2.22c 22.64 ± 3.18b 0.46 ± 0.08a 1.22 ± 0.14b
XL 22.38 ± 3.56c 1363.8 ± 268.7c 18.09 ± 2.06d 14.28 ± 0.96a 1.27 ± 0.85a 89.36 ± 5.69e 4.21 ± 0.32b 1.96 ± 0.23b nd 1.23 ± 0.09b 1.05 ± 0.08bc 40.69 ± 2.59d 29.09 ± 1.75a nd 1.35 ± 0.08ab
MX nd 2638.1 ± 125.04e 246.1 ± 3.16a 5.49 ± 0.55b 0.59 ± 0.06b 98.24 ± 5.57d 2.22 ± 0.16bc 0.73 ± 0.07b 0.73 ± 0.04a 1.52 ± 0.21b 2.11 ± 0.16b 43.93 ± 5.66d 18.77 ± 2.32c nd 1.28 ± 0.11b
HY 32.95 ± 4.27b 3787.3 ± 285.7a 35.72 ± 2.29c 2.82 ± 0.31c 1.17 ± 0.09a 96.33 ± 6.91d 4.41 ± 0.55b 2.06 ± 0.17b 0.59 ± 0.08b 1.56 ± 0.14b 2.44 ± 3.46b 44.71 ± 3.15d 27.74 ± 1.14a nd 2.17 ± 0.31a
RH 2.37 ± 0.45e 2450.2 ± 86.34g 10.51 ± 1.60de 3.51 ± 0.29c 0.89 ± 0.13b 35.38 ± 83.56e 3.42 ± 0.29b 3.21 ± 0.25a nd 1.54 ± 0.18b 2.64 ± 0.39b 13.03 ± 2.97d 19.48 ± 1.18c nd 0.96 ± 0.06c
SM nd 1041.7 ± 122.8b nd 5.64 ± 0.62b 0.54 ± 0.06b 19.86 ± 9.69f 7.35 ± 0.68a 2.38 ± 0.18b nd 0.83 ± 0.11bc 2.07 ± 0.16b 122.14 ± 9.65a 16.92 ± 1.74cd nd 1.32 ± 0.08b
HM 27.84 ± 1.69bc 3391.8 ± 297.9c nd 9.65 ± 0.82ab 0.95 ± 0.12a 87.01 ± 8.24e 3.96 ± 0.26b 3.32 ± 0.31a nd 1.04 ± 0.09b 1.31 ± 0.15bc 42.73 ± 3.17d 30.84 ± 2.32a nd 1.95 ± 0.14a
ST 2.73 ± 0.46e 901.0 ± 42.36j nd nd nd 21.32 ± 1.87h nd nd nd nd nd 9.38 ± 1.12e 19.56 ± 1.14c nd nd
LP 17.09 ± 0.22cd 758.9 ± 108.92k nd nd nd 16.34 ± 0.78g nd nd nd nd 2.27 ± 0.14b 11.18 ± 5.43e nd 0.95 ± 0.06a nd
Int J Food Sci Nutr, Early Online: 1–9
Downloaded by [University of Waterloo] at 07:05 15 October 2015

Juice vesicle
AL 13.93 ± 1.36c 957.4 ± 65.54i nd 9.47 ± 1.38b nd 34.66 ± 4.02e 2.05 ± 0.14e 2.84 ± 0.16a 1.43 ± 0.16a 0.46 ± 0.08b 4.66 ± 0.32a 42.82 ± 3.49h 25.91 ± 3.52d 22.2 ± 1.74d 2.79 ± 0.16b
JW 62.64 ± 4.49a 1790.2 ± 259.4d 46.42 ± 3.26c 19.08 ± 1.15b nd 356.9 ± 3.69a 10.0 ± 0.86a 1.94 ± 0.08a 1.39 ± 0.19a 1.17 ± 0.10a 2.78 ± 0.19b 343.7 ± 26.6a 8.73 ± 5.91f 41.3 ± 2.65b 0.59 ± 0.07d
FH 35.03 ± 2.97b 1924.2 ± 135.4c 32.02 ± 2.15d 22.42 ± 1.36c nd 66.68 ± 7.25d 7.83 ± 0.61b 1.04 ± 0.13b nd 0.22 ± 0.12bc 0.56 ± 0.08d 168.0 ± 8.46d 110.2 ± 7.73a 53.86 ± 3.69a 23.12 ± 1.32a
DOI: 10.3109/09637486.2015.1095864

XL 16.45 ± 1.26 1095.5 ± 294.2h nd 33.29 ± 2.45a 1.35 ± 0.10a 60.49 ± 5.54d 8.35 ± 0.57b nd nd 0.74 ± 0.09ab 1.09 ± 0.08c 69.64 ± 3.16e 9.17 ± 0.54f 21.0 ± 1.56d 3.51 ± 0.24b
MX nd 1191.7 ± 168.1g 119.8 ± 9.65a 7.14 ± 0.89cd nd 59.18 ± 4.61de 9.25 ± 0.54a 1.27 ± 0.09ab 0.91 ± 0.07ab 0.67 ± 0.08ab 0.86 ± 0.06a 267.1 ± 33.6c 27.31 ± 4.01d 30.7 ± 3.21d 0.97 ± 0.05c
HY 2.73 ± 0.16f 2699.0 ± 101.5a nd 10.24 ± 0.46d nd 86.64 ± 4.13b 8.36 ± 0.59b 1.23 ± 0.16ab 0.61 ± 0.09b 1.23 ± 0.11a 2.07 ± 0.25b 287.7 ± 15.5b nd 26.0 ± 3.69d nd
RH 13.49 ± 0.25d 980.6 ± 159.6f 37.69 ± 2.29e 7.62 ± 0.82d nd 45.34 ± 6.98c 3.36 ± 0.73c 1.75 ± 0.09a nd 0.53 ± 0.08ab 2.03 ± 0.14b 80.36 ± 7.02e 22.29 ± 0.29d 11.74 ± 2.54c 0.49 ± 0.09d
SM 10.02 ± 1.05e 813.0 ± 285.1e 28.66 ± 1.38f 9.45 ± 0.65cd nd 28.65 ± 6.22de 2.31 ± 0.62cd 1.23 ± 0.16ab nd 0.52 ± 0.08ab 1.53 ± 0.12c 84.3 ± 14.8d 22.45 ± 0.15d 8.81 ± 0.97e 1.17 ± 0.08c
HM 20.77 ± 1.82c 2560.6 ± 358.7b 56.83 ± 4.63b 10.38 ± 0.74c nd 62.39 ± 2.47d 5.13 ± 0.42c 1.49 ± 0.13ab nd 0.32 ± 0.06b 0.75 ± 0.09d 293.8 ± 18.9b 35.58 ± 2.46c 24.02 ± 1.38d 0.78 ± 0.08cd
ST nd 605.8 ± 96.36g nd nd nd 11.09 ± 0.15f 1.52 ± 0.21e nd nd nd nd 61.1 ± 9.36f 40.93 ± 3.28b nd nd
LP nd 482.4 ± 84.46k nd 0.33 ± 0.08e nd 12.89 ± 0.19f 3.41 ± 0.35d nd nd nd 0.69 ± 0.06d 50.7 ± 8.55g 17.97 ± 2.11e nd nd
Seeds
AL 3.56 ± 0.26a 58.8 ± 27.88b 16.41 ± 1.34c 3.56 ± 0.27a nd 19.34 ± 5.05c nd 0.57 ± 0.05b nd 0.66 ± 0.05a 0.73 ± 0.08b 20.66 ± 2.58c 7.57 ± 0.55b 3.65 ± 0.29a 0.67 ± 0.04a
JW 4.02 ± 0.14a 359.5 ± 5.67e 25.28 ± 1.98b 2.96 ± 0.19a nd 189.2 ± 12.38a nd nd 1.28 ± 0.12a 0.99 ± 0.05a 1.97 ± 0.14a 41.75 ± 3.22b 2.67 ± 0.19d nd nd
b
FH 1.71 ± 0.23b 253.3 ± 33.45d 35.03 ± 2.85a 1.43 ± 0.21ab nd 26.63 ± 1.82 0.79 ± 0.11a 0.87 ± 0.09b nd 0.42 ± 0.07a 0.89 ± 0.06ab 31.53 ± 2.64c 5.92 ± 0.34c nd nd
XL 1.04 ± 0.08bc 80.32 ± 6.25f 19.55 ± 2.21c 0.35 ± 0.07b nd 17.86 ± 5.34c nd nd nd 0.72 ± 0.09a 0.75 ± 0.08b 29.47 ± 1.95cd 4.28 ± 0.29c 0.64 ± 0.05b nd
MX nd 153.26 ± 4.21g nd nd nd 25.88 ± 2.31b nd nd nd nd nd 43.19 ± 2.89b nd 1.11 ± 0.09b nd
HY 0.67 ± 0.51c 287.42 ± 31.65c 24.58 ± 3.32b 2.41 ± 0.14a nd 27.33 ± 1.63b nd nd nd 0.78 ± 0.07a 1.87 ± 0.21a 30.46 ± 4.12c 3.95 ± 0.26c nd nd
b
RH nd 87.35 ± 5.12f nd 0.72 ± 0.08b nd 25.43 ± 3.61 nd nd nd nd 0.83 ± 0.05b 27.59 ± 1.64d 2.88 ± 0.31d nd nd
SM 4.04 ± 0.29a 98.88 ± 10.33e 13.57 ± 1.03d 1.42 ± 0.09ab nd 19.36 ± 1.98c nd nd nd 0.64 ± 0.06a 1.08 ± 0.07a 31.54 ± 1.56c 3.22 ± 0.17cd nd nd
HM 1.14 ± 0.11bc 871.6 ± 64.36a 16.44 ± 1.26c 1.19 ± 0.15ab nd 23.66 ± 3.23bc nd nd nd nd 1.49 ± 0.13a 49.25 ± 3.45a nd 0.68 ± 0.06b nd
ST 1.31 ± 0.15b 52.93 ± 8.19g 4.24 ± 0.32e nd nd 5.33 ± 1.21d nd 1.26 ± 0.15a nd nd nd 25.99 ± 1.95d 9.87 ± 0.11a 0.98 ± 0.09b nd
d
LP 1.85 ± 0.14b 107.8 ± 5.47e 1.86 ± 0.16f 1.22 ± 0.16ab nd 3.33 ± 0.98 1.52 ± 0.16a 2.36 ± 0.33a nd nd 0.52 ± 0.06b 15.06 ± 0.63e 4.72 ± 0.34c 1.51 ± 0.12b nd

nd, not detectable. Data are expressed as means ± standard deviation of triplicate samples.
Different superscripts between same fruit part columns represent significant differences between samples (p50.05).
Phenolic compositions and antioxidant activities of grapefruit
5
6 W. Xi et al. Int J Food Sci Nutr, Early Online: 1–9

4500 and there no marked differences were observed in the other fruit
AL
The levels of phenolics (mg/kg FW)
parts.
JW
FH As one of most important classes of compounds possessing
XL specific bioactivity, phenolic acids have attracted recent scientiEc
3000 MX interest (Cheong et al., 2012; Robbins 2003). Bocco et al. (1998)
HY
RH
found that ferulic acid is the main phenolic acid in citrus fruits
SM and that the abundance of phenolic acids in citrus varied as
HM follows: ferulic acid (0.036–1.580 mg/g DW)4sinapic acid
1500 ST (0.030–0.954 mg/g DW)4p-coumaric acid (0.071–0.193 mg/g
LP
DW)4caffeic acid (0.006–0.229 mg/g DW). We recently found
that ferulic acid is also the most abundant phenolic acid in the
peels of wild mandarins fruits. Wang et al. (2008), however,
0
reported that chlorogenic acid rather than ferulic acid is the main
H arin n
N per n
in in
pe in
tin
D utin
io in

ns l
ob n

C G ge in
or ll tin

C ic id
Fe eic id
lic id
id
ne yo
phenolic acid in the peels of citrus fruits, with the phenolic acids
N citri

N eti
es g
ar id
es n

Er osm

n t

en ac
af ac

ru ac
ac
re

Ta ile
hl a re
Si dict
H ge

R
io

og ic
contents varying as follows: chlorogenic acid (145–339 mg/g
i
Er

f
DW)4p-coumaric acid (41.7–346 mg/g DW)4ferulic acid (30.3–
150 mg/g DW)4sinapic acid (10.1–178 mg/g DW)4caffeic acid
Figure 2. Variations pattern of phenolic compounds in different parts of (3.06–80.0 mg/g DW). In the present study, we found that gallic
nine grapefruit and two pummelo varieties. acid was the major phenolic acid in grapefruit, with the following
content order: gallic acid4chlorogenic acid4caffeic acid4
ferulic acid. These differences may be attributed to the genetic
Downloaded by [University of Waterloo] at 07:05 15 October 2015

backgrounds of the citrus species and/or environmental factors.


found that the narirutin contents were 27.6 mg/100 g DW and Polyphenolic compounds are not equally distributed in the
17.1 mg/100 g DW in mandarin and orange pulp, respectively. different parts of citrus fruits. Yusof et al. (1990) found that the
peels were richer in flavonoids than pulp. Jang et al. (2010)
Polymethoxylated flavones contents reported that the essential oil from Buntan peel had higher
flavonoid content than that in extracts of fruit pulp with different
Among the three Polymethoxylated flavones (PMFs) identified in
solvents. Our recent study showed that the Favonoid levels in
the varieties studied, nobiletin and tangeretin were the most
peels were 1–3 times higher than those in pulp (Xi et al., 2014).
abundant PMFs; they were detected in almost all of the grapefruit
Nogata et al. (2006) observed the following ranking of the
varieties and fruit parts tested, except for the albedo. Higher
flavonoid content in different fruit parts: peel4pulp4juice. In
sinensetin was only detected in the flavedo, whereas trace-level or
the present study, the majority of polyphenol compounds were
no sinensetin was detected in the other fruit parts (Table 2). The
distributed in the flavedo, segment membrane and juice vesicles,
nobiletin and tangeretin contents of all grapefruit tested ranged
especially in the flavedo, which is an excellent source of
from nd to 24.58 mg/g DW and nd to 41.55 mg/g DW, respectively.
polyphenols among citrus fruit parts. The polyphenols contents
The highest content of nobiletin was found in Hongmaxu flavedo,
observed in this study decreased as follows: flavedo4segment
and the highest content of tangeretin was found in Jiwei flavedo.
membrane4juice vesicle4albedo4seeds; juice vesicles and
Much higher nobiletin and tangeretin contents were found in the
seeds were also rich in gallic acid. As a hydrolyzed natural
grapefruit flavedo tested compared to the control Shatianyou and
product of tannin, gallic acid significantly affects both the growth
Liangpingyou pummelo flevedo, whereas no significant differ-
and biofilm formation of bacteria (Shao et al., 2015). Though the
ences were found in the other fruit parts of all varieties tested.
polyphenolic compound contents in seeds were less than in other
PMFs are an extremely-potent class of citrus flavonoids that
fruit parts, many previous studies have shown that grapefruit-seed
have a wide range of nutraceutical functions such as anti-cancer,
extract exhibits good antibacterial activity (Gyawali & Ibrahim,
anti-inflammatory and anti-cardiovascular disease properties
2014; Heggers et al., 2002). In the present study, relatively higher
(Asikin et al., 2012; Manthey & Guthrie, 2002; Zhang et al.,
gallic acid content was detected in grapefruit seeds, and Jiwei,
2013). Sun et al. (2013) found that tangeretin was only detected in
Maxu and Hongmaxu seeds may be the good source of
C. grandis cv. Foyou, and nobiletin and tangeretin were only
antibacterial compounds.
detected in C. paradise cv. Huyou. In this study, nobiletin and
tangeretin were the predominant PMFs in all grapefruit tested,
which is consistent with previous results (Xi et al., 2014). Antioxidant capacity
The DPPH assay is widely used to evaluate the ability of plant
Phenolic acid contents
constituents based on their capacity to scavenge the DPPH radical
Among the phenolic acids identified in the varieties tested, generated in the system (Kumaran & Joel Karunakaran, 2007).
including gallic acid, chlorogenic acid, caffeic acid and ferulic The DPPH values of grapefruits and pummelos varied from
acid, gallic acid was the most dominant, followed by chlorogenic 56.85% to 83.87% in flavedos, from 20.59% to 33.51% in albedos,
acid, caffeic acid and ferulic acid. The contents of gallic acid from 14.56% to 58.47% in segment membranes, from 20.51% to
varied from 0.85 to 343.7 mg/g DW in the grapefruit varieties 57.06% in juice vesicles and from 11.52% to 24.02% in seeds
tested, and chlorogenic acid varied from nd to 110.23 mg/g DW; (Table 3). Ruihong flavedo had the highest DPPH values, while
caffeic acid ranged from nd to 53.86 mg/g DW; and ferulic acid its seed had the lowest DPPH values. All flavedos, segment
ranged from nd to 23.12 mg/g DW. Jiwei juice vesicle had the membranes and juice vesicles of grapefruits tested had higher
highest gallic acid content, whereas Fenghongtangmuxun juice DPPH values than the control Shatianyou and Liangpingyou
vesicles had the highest chlorogenic acid, caffeic acid and ferulic pummelos. Except in Aolangbulangke and Hongmaxu albedo,
acid contents. The gallic acid contents of all grapefruit tested were the DPPH values of the other grapefruit segment membranes
significantly higher than those in the control Shatianyou and were also higher than in the two control pummelos. In seeds, only
Liangpingyou pummelos. In all of the different fruit parts of five out of nine grapefruits tested, including Jiwei,
grapefruit tested, juice vesicle had the highest gallic acid content, Fenghongtangmuxun, Xinglubi, Maxu and Hongmaxu had
DOI: 10.3109/09637486.2015.1095864 Phenolic compositions and antioxidant activities of grapefruit 7

0.49 ± 0.10d

1.47 ± 0.10b
1.47 ± 0.06b
1.12 ± 0.09b
1.17 ± 0.07b
0.62 ± 0.05d
0.65 ± 0.11d

0.35 ± 0.06d
1.02 ± 0.09c

2.01 ± 0.33a
0.98 ± 0.32c
higher DPPH values than those of the control pummelo. The order

FRAP
of DPPH values for the different fruit parts was essentially as
follows: flavedo4segment membrane4juice ves-
icle4albedo4seed. This is similar to the observations of Jang

2.73 ± 0.24b
2.15 ± 0.14b

1.50 ± 0.18d
3.27 ± 0.15a
1.50 ± 0.20c
1.53 ± 0.42c
1.74 ± 0.56c

1.89 ± 0.07c

3.46 ± 0.57a
1.79 ± 0.25c
2.09 ± 0.08c
et al. (2010), who reported that the antioxidant properties of

ABTS
Seeds
Buntan pummelo peel were significantly higher than those of its
pulp using the DPPH method.
The ABTS method is also commonly used to study the

19.43 ± 1.32b
19.56 ± 0.90b
15.56 ± 0.76d
20.68 ± 0.42b
14.80 ± 1.06d
11.52 ± 0.17d
17.74 ± 0.84c

15.36 ± 0.54c
24.02 ± 1.79a
18.14 ± 2.39c
16.76 ± 1.66c
antioxidant capacity of plants based on the capacity to scavenge
DPPH

the radical cation ABTS+ generated in the system (Kim et al.,


2002). The ABTS values of the grapefruits and pummelos varied
from 5.13 mM to 7.99 mM in flavedos, from 3.23 mM to 4.79 mM
2.37 ± 0.16b
1.73 ± 0.18b
2.67 ± 0.18b
2.56 ± 0.04b

1.75 ± 0.24d
2.70 ± 0.32b

1.00 ± 0.17d
1.41 ± 0.14c
3.35 ± 0.17a

1.32 ± 0.16c

1.99 ± 0.13c
in albedos, from 5.39 mM to 7.79 in segment membranes, from
FRAP

3.83 mM to 6.39 mM in juice vesicles and from 1.50 mM to


3.46 mM in seeds (Table 3). The highest ABTS value was
detected in Sibeitimaxu flavedo, whereas the lowest ABTS value
4.09 ± 0.20b

2.11 ± 0.10b
3.57 ± 0.14b

4.23 ± 0.11b
3.75 ± 0.08c
6.05 ± 0.13a

5.82 ± 0.07a
5.69 ± 0.34a
5.94 ± 0.21a

6.39 ± 0.10a
3.83 ± 0.28c
Juice vesicle

was found in Jiwei seed. All flavedos, segment membranes and


ABTS

juice vesicles of grapefruits tested had higher ABTS values than


the control Shatianyou and Liangpingyou pummelos.
Aolangbulangke, Jiwei, Maxu, Sibeitimaxu and Hongmaxu
35.20 ± 0.97b

34.68 ± 0.27b
24.42 ± 1.49d

37.34 ± 2.54b

26.60 ± 1.80d
29.32 ± 1.28c
57.06 ± 0.46a

29.13 ± 0.84c

28.70 ± 0.24c

20.51 ± 3.86e
26.88 ± 0.54

albedos had higher ABTS values than that of the two control
Downloaded by [University of Waterloo] at 07:05 15 October 2015

DPPH

pummelos. Similarly, only Aolangbulangke, Maxu, Huoyan,


Sibeitimaxu and Hongmaxu seeds had higher ABTS values than
seeds of the control Shatianyou and Liangpingyou pummelos.
1.48 ± 0.19bc

1.60 ± 0.23bc

Jiwei juice vesicle also had the highest ABTS value.


2.77 ± 0.23d

3.67 ± 0.07b

3.87 ± 0.28b
2.00 ± 0.37b
6.27 ± 0.03a

3.19 ± 0.33c

3.30 ± 0.26c
1.54 ± 0.11e
1.80 ± 0.29e
FRAP

The FRAP assay is typically used to measure the capacity of


the sample to reduce the ferric complex to the ferrous form
(Contreras-Calderón et al., 2011). The FRAP values of grapefruits
Segment membrane

and pummelos varied from 2.86 mM to 6.52 mM in flavedos, from


5.39 ± 0.10b

6.94 ± 0.19b
4.74 ± 0.12d
4.79 ± 0.25d

4.63 ± 0.46d
5.83 ± 0.17c
7.51 ± 0.21a
7.38 ± 0.06a

7.38 ± 0.04a

7.50 ± 0.24a

5.39 ± 0.09c
ABTS

1.00 mM to 3.15 mM in albedos, from 1.54 mM to 6.27 mM in


segment membranes, from 1.00 mM to 3.15 mM in juice vesicles
and from 0.35 mM to 2.01 mM in seeds (Table 3). Jiwei flavedo
35.61 ± 3.93d
44.17 ± 2.38b

36.63 ± 0.90d
44.69 ± 1.40b

44.90 ± 0.73b
14.56 ± 1.49g
39.52 ± 0.81c

58.47 ± 1.37a
35.39 ± 2.44c

32.85 ± 1.59e

had the highest FRAP values, while Liangpingyou seed had the
17.77 ± 0.38f
DPPH

lowest FRAP value. All flavedos, abedos, segment membranes


Different superscripts between columns represent significant differences between samples (p50.05).

and juice vesicles of grapefruits tested had higher FRAP values


than in the control Shatianyou and Liangpingyou pummelos.
Table 3. Antioxidant capacities of different parts of nine grapefruit and two pummelo varieties.

Except for Ruihong, all flavedos of the grapefruits tested had


1.09 ± 0.14d

2.37 ± 0.16b

2.67 ± 0.18b
2.56 ± 0.04b
1.32 ± 0.16b

2.70 ± 0.32b

1.00 ± 0.17d
3.15 ± 0.17a

1.73 ± 0.18c

1.75 ± 0.24c

1.99 ± 0.13c
FRAP

higher FRAP values than the two control pummelos. Similar to


the DPPH results, the majority of flavedos had higher FRAP
values than their pulps, which agrees with the results obtained by
Jang et al. (2010). Jiwei juice vesicle had higher DPPH, ABTS
3.70 ± 0.30b
1.21 ± 0.11b

3.90 ± 0.14b
2.59 ± 0.32b
2.34 ± 0.08b
3.70 ± 0.41b

3.23 ± 0.06b
2.39 ± 0.12c
4.79 ± 0.05a

4.40 ± 0.03a

2.47 ± 0.17c
ABTS
Albedo

and FRAP value than the other varieties tested, which is


consistent with its rich content of phenolic acids; and it is
DPPH, FRAP and ABTS were expressed as %, mM and mM VC/g DW.

therefore as good source of natural polyphenols.


Data are expressed as means ± standard deviation of triplicate samples.
28.19 ± 0.31b

29.14 ± 0.70b
27.47 ± 3.63b
28.95 ± 1.37b
21.83 ± 1.76d
27.26 ± 1.22b
20.59 ± 0.97c
33.44 ± 2.34a

33.51 ± 0.89a

20.80 ± 0.90c
24.54 ± 1.83c
DPPH

Conclusion
The phenolic composition and antioxidant capacities of different
fruit part of nine grapefruits varieties are reported for the first
3.59 ± 0.13d

5.27 ± 0.54b
3.01 ± 0.18d
2.10 ± 0.43b
5.68 ± 0.91b
3.04 ± 0.08d
2.14 ± 0.31e
6.52 ± 0.12a
4.36 ± 0.50c

4.03 ± 0.31c

2.86 ± 0.20e

time. Naringin, nobiletin and gallic acid were the major phenolic
FRAP

compounds in the samples studied. Naringin was the predominant


flavanone in grapefruit, ranging from 50.18 to 5666.82 mg/g DW.
The highest value was found in Fenghongtangmuxun flavedo.
6.20 ± 0.16b

6.76 ± 0.17b

4.99 ± 0.07d

6.29 ± 0.35b
5.13 ± 0.17d
7.88 ± 0.11a

5.87 ± 0.16a
7.47 ± 0.01a
7.71 ± 0.13a
5.56 ± 0.07c

7.72 ± 0.08a

Jiwei was rich in eriocitrin (4.02–125.39 mg/g DW) and


Flavedo

ABTS

neohesperedin (189.15–1022 mg/g DW). Nobiletin was the major


PMFs, ranging from nd to 24.58 mg/g DW. The highest content of
nobiletin was found in Hongmaxu flavedo. Gallic acid was the
79.16 ± 0.46b

79.20 ± 1.37b
64.73 ± 0.83d
67.96 ± 2.98c
83.87 ± 0.89a

56.85 ± 1.83e
82.21 ± 1.51a
81.54 ± 0.67a
62.60 ± 1.13a
56.41 ± 0.43e

56.79 ± 1.84e

most dominant phenolic acid, ranging from nd to 343.7 mg/g.


DPPH

Jiwei juice vesicle had the highest gallic acid content, while
Fenghongtangmuxun juice vesicle had the highest chlorogenic
acid (110.23 mg/g DW), caffeic acid (53.86 mg/g DW) and ferulic
Abbreviation

acid (23.12 mg/g DW) contents. Compared to the two control


MX

HM
HY

SM
RH
AL

XL
JW
FH

ST
LP

pummelos, Jiwei, Fenghongtangmuxun, Maxu, Huoyan and


Hongmaxu not only had significantly higher polyphenol contents
but also exhibited higher antioxidant capacities. Flavedo had the
No.

highest flavonoid content, while juice vesicle had the highest


1
2
3
4
5
6
7
8
9
10
11
8 W. Xi et al. Int J Food Sci Nutr, Early Online: 1–9

phenolic acid content. The order of polyphenol contents and Goulas V, Manganaris GA. 2012. Exploring the phytochemical content
antioxidant capacities for the different fruit parts was largely as and the antioxidant potential of Citrus fruits grown in Cyprus. Food
follows: flavedo4segment membrane4juice vesicle4albedo4 Chem 131:39–47.
Gyawali R, Ibrahim SA. 2014. Natural products as antimicrobial agents.
seed. Our findings provide useful information for future studies Food Control 46:412–429.
and for utilization of grapefruit germplasm in China and abroad. Heggers JP, Cottingham J, Gusman J, Reagor L, Mccoy L, Carino E,
Cox R, Zhao JG. 2002. The effectiveness of processed grapefruit-seed
extract as an antibacterial agent: II. Mechanism of action and in vitro
Declaration of interest toxicity. J Altern Complement Med 8:333–340.
Jang HD, Chang KS, Chang TC, Hsu CL. 2010. Antioxidant potentials of
The authors report no conflicts of interest. The authors alone are buntan pummelo (Citrus grandis Osbeck) and its ethanolic and
responsible for the content and writing of this article. This work acetified fermentation products. Food Chem 118:554–558.
was supported by the Natural Science Foundation of Chongqing Jing L, Lei ZT, Zhang GW, Pilon A, Huhman D, Xie RJ, Xi WP, et al.
City (cstc2013jcyjA80012), the Fundamental Research Funds 2015. Metabolite profiles of essential oils in citrus peels and their
for the Central Universities (XDJK2014A014), the Program for taxonomic implications. Metabolomics 11:952–963.
Chongqing Innovation Team of University (KJTD201333), and Kelebek H, Canbas A, Selli S. 2008. Determination of phenolic
composition and antioxidant capacity of blood orange juices obtained
the ‘111’ Project (B12006).
from cvs. Moro and Sanguinello (Citrus sinensis (L.) Osbeck) grown in
Turkey. Food Chem 107:1710–1716.
Khan MK, Zill EH, Dangles OA. 2014. Comprehensive review on
References flavanones, the major citrus polyphenols. J Food Compos Anal 33:
Abad-Garcia B, Garmon-Lobato S, Berrueta LA, Gallo B, Vicente F. 85–104.
2012. On line characterization of 58 phenolic compounds in Citrus Kim DO, Lee KW, Lee HJ, Lee CY. 2002. Vitamin C equivalent
Downloaded by [University of Waterloo] at 07:05 15 October 2015

fruit juices from Spanish cultivars by high-performance liquid antioxidant capacity (VCEAC) of phenolic phytochemicals. J Agric
chromatography with photodiode-array detection coupled to electro- Food Chem 50:3713–3717.
spray ionization triple quadrupole mass spectrometry. Talanta 99: Kumaran A, Joel Karunakaran R. 2007. In vitro antioxidant activities of
213–224. methanol extracts of five Phyllanthus species from India. LWT-Food
Asikin Y, Taira I, Inafuku-Teramoto S, Sumi H, Ohta H, Takara K, Sci Technol 40:344–352.
Wada K. 2012. The composition of volatile aroma components, Manthey JA, Guthrie N. 2002. Antiproliferative activities of citrus
flavanones, and polymethoxylated flavones in shiikuwasha (Citrus flavonoids against six human cancer cell lines. J Agric Food Chem 50:
depressa Hayata) peels of different cultivation lines. J Agric Food 5837–5843.
Chem 60:7973–7980. Njoroge SM, Koaze H, Karanja PN, Sawamura M. 2005. Volatile
Barreca D, Bellocco E, Caristi C, Leuzzi U, Gattuso G. 2010. Flavonoid constituents of redblush grapefruit (Citrus paradisi) and pummelo
composition and antioxidant activity of juices from Chinotto (Citrus (Citrus grandis) peel essential oils from Kenya. J Agric Food Chem 53:
myrtifolia Raf.) fruits at different ripening stages. J Agric Food Chem 9790–9794.
58:3031–3036. Nogata Y, Sakamoto K, Shiratsuchi H, Ishii T, Yano M, Ohta H. 2006.
Barreca D, Bellocco E, Caristi C, Leuzzi U, Gattuso G. 2011. Elucidation Flavonoid composition of fruit tissues of citrus species. Biosci
of the flavonoid and furocoumarin composition and radical-scavenging Biotechnol Biochem 70:178–192.
activity of green and ripe chinotto (Citrus myrtifolia Raf.) fruit tissues, Oboh G, Ademosun AO. 2011. Phenolic extracts from grapefruit peels
leaves and seeds. Food Chem 129:1504–1512. (Citrus paradisi) inhibit key enzymes linked with type 2 diabetes and
Bocco A, Cuvelier ME, Richard H, Berset C. 1998. Antioxidant activity hypertension. J Food Biochem 35:1703–1709.
and phenolic composition of citrus peel and seed extracts. J Agric Food Ooghe WC, Ooghe SJ, Detavernier CM, Huyghebaert A. 1994.
Chem 46:2123–2129. Characterization of orange juice (Citrus sinensis) by flavanone
Cano A, Medina A, Bermejo A. 2008. Bioactive compounds in different glycosides. J Agric Food Chem 42:2183–2190.
citrus varieties, discrimination among cultivars. J Food Compos Anal Peterson JJ, DWyer JT, Beecher GR, Bhagwat SA, Gebhardt SE,
21:377–381. Haytowitz DB, Holden JM. 2006. Flavanones in oranges, tangerines
Chaudhary P, Jayaprakasha GK, Porat R, Patil BS. 2012. Degreening and (mandarins), tangors, and tangelos: a compilation and review of the
postharvest storage influences ’Star Ruby’ grapefruit (Citrus paradisi data from the analytical literature. J Food Compos Anal 19:S66–S73.
Macf.) bioactive compounds. Food Chem 135:1667–1675. Ramful D, Tarnus E, Aruoma OI, Bourdon E, Bahorun T. 2011.
Cheong MW, Chong ZS, Liu SQ, Zhou W, Curran P, Bin Y. 2012. Polyphenol composition, vitamin C content and antioxidant capacity of
Characterisation of calamansi (Citrus microcarpa). Part I: volatiles, Mauritian citrus fruit pulps. Food Res Int 44:2088–2099.
aromatic profiles and phenolic acids in the peel. Food Chem 134: Robbins RJ. 2003. Phenolic acids in foods: an overview of analytical
686–695. methodology. J Agric Food Chem 51:2866–2887.
Choi HS, Song HS, Ukeda H, Sawamura M. 2000. Radical-scavenging Shao D, Li J, Li J, Tang R, Liu L, Shi J, Huang Q, Yang H. 2015.
activities of citrus essential oils and their components: detection using Inhibition of gallic acid on the growth and biofilm formation of
1,1-diphenyl-2-picrylhydrazyl. J Agric Food Chem 48:4156–4161. Escherichia coli and Streptococcus mutans. J Food Sci 80:
Contreras-Calderón J, Calderón-Jaimes L, Guerra-Hernández E, Garcı́a- M1299–M1305.
Villanova B. 2011. Antioxidant capacity, phenolic content and vitamin Sun YJ, Qiao LP, Shen Y, Jiang P, Chen JC, Ye XQ. 2013. Phytochemical
C in pulp, peel and seed from 24 exotic fruits from Colombia. Food profile and antioxidant activity of physiological drop of citrus fruits.
Res Int 44:2047–2053. J Food Sci 78:C37–C42.
Del Rı́o JA, Fuster MD, Gómez P, Porras I, Garcı́a-Lidón A, Ortuño A. Tripoli E, Guardia ML, Giammanco S, Majo DD, Giammanco M. 2007.
2004. Citrus limon: a source of flavonoids of pharmaceutical interest. Citrus flavonoids: molecular structure, biological activity and nutri-
Food Chem 84:457–461. tional properties: a review. Food Chem 104:466–479.
de Moraes A, dos Santos Soares Filho W, Guerra M. 2007. Karyotype Wang YC, Chuang YC, Hsu HC. 2008. The flavonoid, carotenoid and
diversity and the origin of grapefruit. Chromosome Res 15:115–121. pectin content in peels of citrus cultivated in Taiwan. Food Chem 106:
Du Q, Chen H. 2010. The methoxyflavones in Citrus reticulata Blanco 277–284.
cv. ponkan and their antiproliferative activity against cancer cells. Food Xi WP, Fang B, Zhao QY, Jiao BN, Zhou ZQ. 2014. Flavonoid
Chem 119:567–572. composition and antioxidant activities of Chinese local pummelo
Folimonova SY, Robertson CJ, Garnsey SM, Gowda S, Dawson WO. (Citrus grandis Osbeck.) varieties. Food Chem 161:230–238.
2009. Examination of the responses of different genotypes of citrus to Yamada T, Hayasaka S, Shibata Y, Ojima T, Saegusa T, Gotoh T,
Huanglongbing (citrus greening) under different conditions. Ishikawa S, et al. 2011. Frequency of citrus fruit intake is associated
Phytopathology 99:1346–1354. with the incidence of cardiovascular disease: the Jichi Medical School
Girennavar B, Jayaprakasha GK, Jifon J, Patil B. 2008. Variation of cohort study. J Epidemiol 21:169–175.
bioactive furocoumarins and flavonoids in different varieties of Yusof S, Ghazali HM, King GS. 1990. Naringin content in local citrus
grapefruits and pummelo. Eur Food Res Technol 226:1269–1275. fruits. Food Chem 37:113–121.
DOI: 10.3109/09637486.2015.1095864 Phenolic compositions and antioxidant activities of grapefruit 9
Zhang H, Xi WP, Zhou ZQ, Wang HL, Ba ZC. 2013. Bioactivities and wild mandarin (Citrus reticulata Blanco) fruits. Food Chem 145:
structure of polymethoxylated flavones in citrus. J Food Agric Environ 674–680.
11:237–242. Zhang YM, Zhou ZQ, Sun YJ, Shen Y, Zhong LZ, Qiao LP. 2011b.
Zhang MX, Duan CQ, Zang YY, Huang ZW, Liu GJ. 2011a. Simultaneous determination of 18 Favonoids in citrus fruits by high-
The flavonoid composition of flavedo and juice from the performance liquid chromatography. J Integr Agric 45:3558–3565. In
pummelo cutivar (Citrus grandis (L.) Osbeck) and the Chinese).
grapefruit cutivar (Citrus paradisi) from China. Food Chem 129: Zhao H, Sun R, Albrecht U, Padmanabhan C, Wang A, Coffey MD, Girke
1530–1536. T, et al. 2013. Small RNA profiling reveals phosphorus deficiency as a
Zhang YM, Sun YJ, Xi WP, Shen Y, Qiao LP, Zhong LZ, Ye XQ, Zhou contributing factor in symptom expression for citrus huanglongbing
ZQ. 2014. Phenolic compositions and antioxidant capacities of Chinese disease. Mol Plant 6:301–310.

Supplementary material available online


Supplementary Figure S1
Downloaded by [University of Waterloo] at 07:05 15 October 2015

You might also like