Journal of Integrative Agriculture 2019, 18(5): 1148–1158

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RESEARCH ARTICLE

Comparison of phenolic profiles and antioxidant activities in skins

and pulps of eleven grape cultivars (Vitis vinifera L.)

LI Fu-xiang1, LI Fu-hua1, 2, YANG Ya-xuan1, YIN Ran3, MING Jian1, 2

1
College of Food Science, Southwest University, Chongqing 400715, P.R.China
2
Research Center of Food Storage & Logistics, Southwest University, Chongqing 400715, P.R.China
3
Ernest Mario School of Pharmacy, Rutgers University, NJ 008854, USA

Abstract
Eleven grape cultivars were analysed to explore the variety differences of fresh grape phenolic profiles. The results
showed that free phenolics were predominant in grape skins and pulps, and showed the higher antioxidant activities than
bound. In 11 cultivars, Muscat Kyoho extracts had the highest total phenolic content in skins (10.525 mg GAE g–1 FW)
and pulps (1.134 mg GAE g–1 FW), and exhibited the highest DPPH radical scavening capacity (EC50=11.7 µg mL–1) and
oxygen radical absorbance capacity (ORAC) value (190.57 µmol TE g–1 FW) of free phenolic in skin. In addition, the most
abundant phenolics in grape skins were found to be flavonoids such as kaempferol in Kyoho skin (541.2 µg g–1 FW), rutin,
catechin and epicatechin in Muscat Kyoho skin (262.3, 86.3 and 70.0 µg g–1 FW, respectively). Furthermore, the principal
component analysis showed a strong difference of phenolic profiles with the cultivars, existing forms and distributions.
Pearson correlation coefficient analysis showed a significant linear correlation between total phenolic content and antioxidant
activity (P<0.05). Therefore, both skins and pulps were rich sources of bioactive phenolic compounds, and Muscat Kyoho
was the ideal source among all samples.

Keywords: grape phenolics, varietal diversity, antioxidant activity, principal component analysis

minerals, etc.) and bioactive compounds (phenolic acids,

1. Introduction
Grape (Vitis vinifera L.) has a long history of cultivation and
consumption. Fresh grape is rich in nutrients (dietary fiber,
Received 12 July, 2018 Accepted 30 September, 2018
LI Fu-xiang, E-mail: fuxianglee93@163.com; Correspondence
MING Jian, Tel: +86-23-68251298, Fax: +86-23-68251947,
E-mail: mingjian1972@163.com, food_mj@swu.edu.cn
© 2019 CAAS. Published by Elsevier Ltd. This is an open
access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).
doi: 10.1016/S2095-3119(18)62138-0
flavonoids, isoflavonoids, thiols, carotenoids, ascorbic acid,
tocopherols, etc.) (Yang and Xiao 2013; Fabani et al. 2017).
Phenolic compounds as one kind of phytochemicals have
various nutritional and healthy properties, such as antibacterial,
anti-inflammatory, hypoglycemic, and hypolipidemic activities
(Kemperman et al. 2013; Jara-Palacios et al. 2014; Shahidi
and Ambigaipalan 2015). Extensive literatures investigated
the phenolic content and antioxidant capacity of grape
products, especially wine and raisin (Jacob et al. 2008; Fang
et al. 2010; Williamson and Carughi 2010; Meng et al. 2011;
De Castilhos et al. 2017). However, information on the
phenolic profile of fresh grape is scarce.
The phenolic profiles of grapes depend on various factors
such as variety, maturity (Fanzone et al. 2011), genetic
 LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158
diversity (Bustamante et al. 2017), viticulture practices
(De Pascali et al. 2014), soil characteristics (Cheng et al.
2015), environmental stress and vine health status (Rusjan
et al. 2012). The phenolic composition of grapes strongly
depends on grape varieties (Yang and Xiao 2013; Aubert
and Chalot 2018). The (+)-catechin content of cv. Muscat de
Hambourg (19.3 mg kg–1 fresh weight (FW) of samples) was
higher than that of cv. Italia (3.1 mg kg–1 FW), the caftaric
acid content of cv. Alphonse Lavallée (93.8 mg kg–1 FW)
was higher than cv. Centennial Seedless (25.6 mg kg–1 FW)
(Aubert and Chalot 2018). The grape quality and sensory
properties are significantly affected by grape varieties
(Aubert and Chalot 2018). Therefore, it is essential to study
the influence of grape varieties on the phenolic profiles.
Distribution of phenolic compounds in grape is uneven.
About 64% of total free phenolic compounds are in the
seeds, 30% are in the skin, and 6% are in the pulp. Phenolic
compounds in the seeds, skin and pulp are represented
by flavan-3-ols, flavonols and hydroxycinnamic acids,
respectively (Teixeira et al. 2013; Yilmaz et al. 2014).
The phenolic compounds in fruits are in both free and
bound forms. Bound phenolics, are mainly associated with
the cell wall material, and cannot be digested through the
stomach and small intestine but reach the colon completely,
where they are released to exhibit bioactivity with health
benefits. Most of studies investigated the free phenolics of
grape (Sun et al. 2002; Teixeira et al. 2013; Yilmaz et al. 2014;
Belviso et al. 2017; Aubert and Chalot 2018). The bound
phenolic profiles of grapes still remain unclear.
The objective of this study is to: (1) investigate the
composition and distribution of free and bound phenolic
compounds, as well as their antioxidant activities in skins
and pulps of 11 grape cultivars; (2) evaluate the correlation
between the phenolic compounds and antioxidant activities
by the principal component analysis (PCA) and the Pearson
correlation coefficient method.
2. Materials and methods
2.1. Materials
1,1-Diphenyl-2-picrylhydrazyl (DPPH), 6-hydroxy-2,5,7,8-
tetramethylchroman-2-carboxylic acid (Trolox), as well as
phenolic standards were purchased from Sigma-Aldrich
(St. Louis, MO, USA), and the purity of each compound
was >98%. 2,2´-Azobis (2-methylpropionamidine)
dihydrochloride (ABAP) was purchased from Tokyo
Chemical Industry (Tokyo, Japan). Acetonitrile (HPLC
grade) and formic acid (HPLC grade) were obtained from
Tianjin Shield Fine Chemicals Company (Tianjin, China).
Other chemicals were of analytical grade.
1149
2.2. Grape samples
Grapes with a characteristic scent were harvested in August
2017 from the Experimental Farm of Southwest University,
Chongqing, China. The pictures, flavor characteristics and
other information of the collected grapes were summarized
in Table 1. Fresh grapes were picked randomly distributed
throughout different vines at the appropriate ripeness, and
then packed in black polyethylene bags. For each cultivar,
skins (30 g) and pulps (75 g) were separately packed, and
then stored in the dark at –40°C until analysis within three
weeks.
2.3. Determination of the soluble solid content (SSC),
titratable acidity (TA) and SSC/TA ratio
The SSC, TA and SSC/TA ratio were measured using
the method described by Ali et al. (2016) with a slight
modification. The SSC was measured with PAL-2 digital
refrectometer (Atago Co., Japan) and expressed as the
percent. TA was determined by the titration of grape juice
against 0.01 mol L–1 NaOH, and given as the percent of
tartaric acid. The SSC/TA ratio was calculated by dividing
SSC with corresponding TA value of the grape sample.
2.4. Extraction of free and bound phenolics
Grape skins and pulps were prepared according to the
method described by Sun et al. (2002) and Wolfe et al.
(2003) with a slight modification. Briefly, the fresh pulps
(25 g) or skins (10 g) were extracted with 50 mL chilled
acetone solution (80%, v/v), respectively. The mixture
was homogenized for 10 min at 10 000 r min–1 by a high
speed dispersator (XHF-D; Ningbo Scientz Instrument Co.,
China). The supernatant was collected. The residue was
re-extracted twice with the same procedures. All filtrate
was collected and evaporated at 45°C until approximately
90% of the filtrate was evaporated by a rotovapor (RE-
52AA; Shanghai Yarong Instrument Co., China). The free
phenolic extracts were recovered with water to a final
volume of 25 mL. The soluble free phenolic extracts were
stored at –40°C until analysis within three weeks. The
residues from the above soluble free phenolic extraction
were digested with 20 mL (2 mol L–1) NaOH for 90 min
with shaking in darkness. The mixture was acidified to
pH=2 with concentrated HCl, and extracted for five times
with 100 mL ethyl acetate. The ethyl acetate fraction
was evaporated at 45°C to dryness. The bound phenolic
extracts were reconstituted in 10 mL of water and stored
at –40°C until analysis within three weeks.
1150 LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158

Table 1 The grape varieties investigated

Variety Name Presence of seed Flavor characteristic Original location
Gold Finger (Vitis vinifera L.×V. labrusca L.) Exist Rock candy flavor, milk flavor Japan

Hakuho (V. vinifera L.×V. labrusca L.) Exist Strawberry flavor Japan

White Olympia (V. vinifera L.×V. labrusca L.) Exist Banana flavor Japan

Shine Muscat (V. vinifera L.×V. labrusca L.) Exist Rose flavor Japan

Kyoho (V. vinifera L.×V. labrusca L.) No Strawberry flavor Japan

Muscat Kyoho (V. vinifera L.×V. labrusca L.) Exist Rose flavor China

Beni Fuji (V. vinifera L.×V. labrusca L.) No Creamy Japan

Red Bharati (V. vinifera L.) Exist No flavor Japan

Summer Black (V. vinifera L.×V. labrusca L.) No Strawberry flavor Japan

Hutai-8 (V. vinifera L.×V. labrusca L.) Exist Rose flavor China

Moldova (V. vinifera L.) No Strawberry flavor Moldova

2.5. Determination of the phenolic content
The contents of free and bound phenolics in grapes were
measured by the Folin-Ciocalteu colorimetric method
as reported previously (Singleton et al. 1999) with a
slight modification. Briefly, 0.2 mL of the appropriate
dilutions of extracts and 0.8 mL water were mixed. Then,
0.2 mL Folin-Ciocalteu reagent was added. After 6 min,
the reaction was neutralized with sodium carbonate (2 mL,
7%, w/v), and 1.6 mL water was then added. The samples
were given the resting time for 90 min in darkness. The
absorbances of samples were measured at 760 nm by
a UV-vis spectrophotometer (UV-722; Shanghai Jinghua
Instrument Co., China). The gallic acid was the standard.
The phenolic content was expressed as milligram gallic
acid equivalents per gram of grape in fresh weight (mg
GAE g–1 FW).
et al. 2010; Sandhu and Gu 2010). The HPLC system
was consist of Shimadzu LC-20AD pump, Shimadzu
SIL-20A autosampler, and a Shimadzu SPD-M20A diode
array detector (DAD). The grape phenolic extracts
were analysed on a Hypersil BDS C 18 column (5 µm,
250 mm×4.6 mm i.d.; Thermo Fisher Scientific, New York,
USA) with the column temperature 40°C and the flow rate of
0.7 mL min–1. The gradient system included: A, water
including 0.1% formic acid; B, acetonitrile. The elution
program was the following: 10% B at 0–5 min; 10–40% B
at 5–50 min; 40–90% B at 50–55 min; 90% B at 55–62 min;
90–10% B at 62–65 min; 10% B at 65–75 min. The injection
volume was 20 µL. The wavelength range of scanning was
190–800 nm, and wavelength at 280 nm was analyzed.
Phenolic compounds were identified by comparing the
retention time in specific wavelength spectra with those of
authentic standards.

2.6. Phenolic profiles analysis by HPLC-DAD 2.7. Antioxidant activity analyses

Phenolic compounds were determined by a Shimadzu Free radical scavenger assay The free radical scavenging
HPLC system that performed as described previously (Iii capacity of grape extracts were measured based on the
 LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158
method (Brand-Williams et al. 1995; Li et al. 2013) with a
slight modification. Briefly, 1 mL extract was mixed with the
stock solution of DPPH (5 mL, 0.1 mmol L–1) freshly prepared
in ethanol. After keeping in the dark at 20°C for 30 min,
the absorbance was then measured at 517 nm by a UV-vis
spectrophotometer (UV-722; Shanghai Jinghua Instrument
DPPH-free radical scavenging activity (%)=[1–(Asample–Ablank)/ADPPH]×100
The extract concentration providing 50% of DPPH free
radicals scavenging activity (EC50) was calculated by plotting
the scavenging activity percentage against the extract
concentration. Where, Asample, Ablank and ADPPH, are the
absorbance of sample, distilled water and DPPH solution,
respectively.
Oxygen radical absorbance capacity assay The oxygen
radical absorbance capacity (ORAC) of extracts were
measured by the method reported by Wolfe et al. (2008) with
a slight modification. In brief, grape extracts were diluted by
75 mmol L–1 phosphate buffer (pH 7.4) with the appropriate
concentration (20 µL/well) to a 96-well black microplate in
triplicate. The microplate was then incubated at 37°C for
10 min, and mixed with 0.96 mmol L–1 fluorescein (200 µL/
well). Reactions were incubated at 37°C for 20 min, then
adding 119.4 mmol L–1 ABAP (20 µL/well). Fluorescence
intensity was recorded immediately at excitation wavelength
of 485 nm and emission of 520 nm for 35 cycles every
4.5 min by Multi-Mode Microplate Reader (Synergy H1 MG;
Biotek, Vermont, USA). Phosphate buffer and trolox were
used as the blank control and standard, respectively. The
ORAC value was expressed as µmol Trolox equivalents
of one gram grape in fresh weight (µmol TE g–1 FW) and
calculted by the eqs. (2) and (3):
AUC=(0.5×f1/f1+f2/f1+f3/f1+...+fn/f1+...+f34/f1+0.5×f35/f1)×CT
(2)
ORAC value=(AUCsample–AUCblank)/(AUCtrolox–AUCblank)(3)
Where, AUC is the area under the fluorescence vs. time
curve, ƒ1 is the first fluorescence recording value, ƒn is the
nth fluorescence recording value, CT is the time of interval
measure.
2.8. Statistical analyses
The statistical significance evaluation of measured
differences were analyzed using one-way analysis of
variance (ANOVA), the differences between means were
performed by Tukey’s multiple comparison test, and
significance was defined as P<0.05 by the SPSS software
20.0 (SPSS Inc., Chicago, IL, USA). All data were reported
as mean±SD for three replications, but not field replicates.
The charts were created using the Sigmaplot software
(Graph Pad Software, San Diego, CA, USA).
Correlation coefficient analysis The Pearson’s coefficient
1151
Co., China). The absorbance of freshly prepared DPPH
solution was measured prior to analysis. The distilled water
and ascorbic acid were used as the blank and standard,
respectively. DPPH antioxidant capacity of the phenolic
extracts was expressed as the percent of DPPH-free radical
scavening activity using the eq. (1):
(1)
of correlation analysis was determined between the contents
of individual phenolic compounds, free and bound phenolics
determined. Correlation significance was defined at the 0.01
or 0.05 level by SPSS Software 20.0 (SPSS Inc., Chicago,
IL, USA).
Principal component analysis Principal component
analysis (PCA) was applied to check for similar characteristics
of samples, as well as to associate response variables by
SPSS software 20.0 (SPSS Inc., Chicago, IL, USA). Data
that contained 11 objects×12 or 16 variables were processed
using the covariance matrix with autoscaling. Where the 11
objects were the number of samples, the variables were the
phenolic compounds and total phenolic contents determined
by HPLC-DAD, and antioxidant activity (DPPH and ORAC).
The initial matrices were 11×16, 11×16, 11×16, and 11×12
for free and bound phenolics of skin and pulp samples,
respectively.
3. Results
3.1. Physicochemical properties of the 11 grape
varieties
Muscat Kyoho showed the highest soluble solid content
(20.18%), Shine Muscat showed the lowest SSC (12.83%),
and the SSC of other grape varities ranged from 14.35 to
18.93% (Appendix A). The titratable acidity (TA) of all the
grape varities ranged from 0.301% (Red Bharati) to 0.553%
(Moldova). Red Bharati exhibited the highest ratio of SSC
to TA (58), and the ratio of the rest grape varities ranged
from 28 (Moldova and White Olympia) to 54 (Muscat Kyoho).
3.2. Total phenolic content (TPC) of the grape skins
and pulps
As shown in Table 2, most of the phenolic compounds were
detected in the skins, whereas very low concentrations in the
pulps. The TPC of grape skins (1.296–10.525 mg GAE g–1
FW) were higher than those of pulps (0.189–1.134 mg GAE
g–1 FW). Muscat Kyoho had the highest TPC in its pulp and
skin, while Shine Muscat had the lowest TPC value. The TPC
of skins were 6.5 to 17.8 times higher than those of pulps.
Free phenolic compounds were the dominant both in pulps
(about 85–98% of TPC) and skins (about 78–97% of TPC).
1152 LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158

Table 2 Phenolic contents of different parts of grape varieties (mg GAE g–1 FW)
Pulps Skins
Variety
Free Bound Total Free Bound Total
Gold Finger 0.567±0.135 bc 0.047±0.005 a 0.578±0.166 bc 3.517±0.129 e 0.271±0.018 cde 3.788±0.111 e
Hakuho 0.498±0.164 bc 0.025±0.004 a 0.524±0.168 bcd 3.886±0.774 e 0.149±0.121 e 4.374±0.591 de
White Olympia 0.309±0.053 cd 0.033±0.015 a 0.343±0.064 cd 5.879±0.353 cd 0.241±0.057 de 6.121±0.326 cd
Shine Muscat 0.170±0.036 d 0.019±0.003 a 0.189±0.033 d 1.017±0.118 f 0.278±0.020 cde 1.296±0.136 f
Kyoho 0.590±0.184 bc 0.089±0.096 a 0.682±0.270 bc 8.159±2.222 b 0.689±0.034 a 8.847±2.256 ab
Muscat Kyoho 1.084±0.164 a 0.050±0.013 a 1.134±0.173 a 10.188±0.772 a 0.337±0.007 bcd 10.525±0.779 a
Beni Fuji 0.289±0.034 cd 0.045±0.012 a 0.327±0.034 cd 4.549±0.807 de 0.719±0.028 a 5.152±1.134 de
Red Bharati 0.592±0.166 bc 0.109±0.027 a 0.701±0.193 bc 8.193±0.313 b 0.627±0.017 a 8.820±0.329 ab
Summer Black 0.679±0.035 b 0.056±0.029 a 0.735±0.063 bc 8.474±0.293 b 0.394±0.045 bc 8.868±0.338 ab
Hutai-8 0.781±0.106 b 0.041±0.002 a 0.823±0.110 b 5.912±0.821 cd 0.359±0.006 bcd 6.271±0.816 cd
Moldova 0.591±0.066 bc 0.026±0.002 a 0.616±0.066 bc 7.542±0.547 bc 0.459±0.083 b 8.002±0.487 bc
Data are mean±SD (n=3). Values with different letters in each column are significantly different (P<0.05).

3.3. Identification and quantitation of phenolic com-
pounds by HPLC
As shown in Table 3 (skins) and Table 4 (pulps), a total of
13 phenolic compounds were detected, including seven
phenolic acids, five flavonoids, and resveratrol.
Phenolic compounds in grape skins As shown in
Table 3, the most abundant phenolics in grape skins were
flavonoids (accounts for 79% of free phenolics and 56% of
bound phenolics). The flavonoids of grapes were strongly
different in grape varieties. This result was in agreement
with that in Di Lecce et al. (2014). For free flavonoids,
kaempferol was the most abundant flavonoids in Kyoho
(541.2 µg g–1 FW), while rutin (262.3 µg g–1 FW), catechin
(86.3 µg g–1 FW) and epicatechin (70.0 µg g–1 FW) were
the most abundant in Muscat Kyoho. Compared to free
flavonoids, the concentrations of bound flavonoids were
lower. For free phenolic acids, the highest concentration
of gallic acid was in White Olympia (81.8 µg g–1 FW). For
bound phenolic acids, gallic acid and caftaric acid were in
all varieties except Beni Fuji and Hutai-8, while caffeic acid
and p-coumaric acid were detected in all varieties. The most
abundant bound resveratrol was in Summer Black (172.6 µg
g–1 FW). The contents of resveratrol were significantly
different (P<0.05), which was in agreement with the result
reported by Okuda and Yokotsuka (1996).
Phenolic compounds in grape pulps The composition of
phenolic compounds in grape pulps was similar to that of
skins. However, the content of phenolic compounds in grape
pulps was lower than that of skins. Phenolic acids were the
most abundant phenolics in grape pulps (accounts for 53%
of free phenolics and 54% of bound phenolics), which was
in accordance with the report (Pantelić et al. 2016). For free
phenolic acids, gallic acid was the most abundant in Gold
Finger (44.9 µg g–1 FW), and caftaric acid was the most
abundant in Hutai-8 (192.3 µg g–1 FW). For free flavonoids,
catechin was the most abundant in Red Bharati (134.5 µg
g–1 FW), and epicatechin was the most abundant in Muscat
Kyoho (45.5 µg g–1 FW). Resveratrol was only determined in
Summer Black and Moldova in minor quantities (1.9 µg g–1
FW). For bound flavonoids, catechin was the most abundant
in Red Bharati (9.8 µg g–1 FW), rutin and isoquercitrin were
not determined in the grape pulps. It suggested that the
phenolic compounds of grape skins and pulps were different
between free and bound forms.
3.4. Antioxidant activities
The DPPH radical scavenging capacity The results of
DPPH radical scavenging capacity of grape extracts were
shown in Fig. 1-A and B for pulps and skins, respectively.
For skins, the free phenolics of Muscat Kyoho presented
the highest radical scavenging capacity (EC50=11.7 µg mL–1),
while Shine Muscat showed the lowest antiradical capacity
(19.2 µg mL–1). However, for the bound phenolics, Shine
Muscat presented the highest radical scavenging capacity
(19.3 µg mL–1), followed by Muscat Kyoho (23.3 µg mL–1).
In general, the DPPH free radical scavenging ability of
free phenolics was about 1.8 times stronger than bound
phenolics in skins.
For pulps, the free phenolics of Beni Fuji presented the
highest antiradical capacity (EC50=14.1 µg mL–1) and stronger
than ascorbic acid (EC50=17.9 µg mL–1), followed by White
Olympia (EC50=17.1 µg mL–1) and Red Bharati (EC50=17.5 µg
mL–1), while Shine Muscat performed the lowest scavenging
capacity (EC 50=33.9 µg mL –1). For bound phenolics,
Moldova presented the lowest EC 50 value of 23.2 µg
mL–1. The DPPH free radical scavenging ability of free
phenolics were about 1.6 times higher than those of bound
phenolics. The free phenolics and bound phenolics in skins
exhibited higher antiradical capacity than these in pulps.
Generally, Muscat Kyoho, Beni Fuji and Red Bharati took
advantages in scavenging DPPH free radical.
The oxygen radical absorbance capacity (ORAC) As
Table 3 Contents of phenolic acids, selected flavonoids, and resveratrol of grape skins (µg g–1 FW)1)
Phenolic acids Flavonoids
Variety RES Total
GA CAT DHB VA CAF SYA p-CMA C EC RT IQE KAE
Free phenolics
Gold Finger 56.4±3.9 b 22.2±0.8 c – 7.7±0.3 e – 4.1±0.0 d – 28.7±0.9 de – 99.2±5.2 cd 31.9±3.2 c 120.2±27.6 g 370.3±40.3 e
Hakuho 17.1±0.4 de 47.1±2.5 a – – 12.4±0.5 bc – – – 22.7±4.4 bc 73.7±7.0 de 40.8±6.1 c 199.0±24.4 efg – 412.8±39.4 e
White Olympia 81.8±8.9 a 37.6±1.7 b 20.1±0.6 a 16.1±1.8 cd 11.4±0.2 bc – – 45.2±1.1 cd 31.7±3.8 b 17.5±4.5 f 33.0±4.5 c 433.1±10.4 bc – 727.6±7.4 cd
Shine Muscat 6.5±2.5 efg 8.0±0.1 e 13.5±0.3 c – – – – 18.1±0.3 e – 53.2±6.8 ef 4.4±0.2 c 29.1±2.4 h – 132.9±11.8 f
Kyoho 11.2±0.5 defg 15.2±0.5 cde 15.8±0.4 b 18.5±0.1 c – 9.2±0.1 bc 3.7±0.3 a 52.1±4.9 bc – 98.0±10.2 cd 45.9±1.0 c 541.2±24.3 a 33.4±2.9 c 844.3±31.3 bc
Muscat Kyoho 10.1±1.0 defg 12.9±0.4 de – 35.6±1.2 b 14.9±0.4 b 18.2±0.2 a – 86.3±4.4 a 70.0±0.6 a 262.3±21.9 a 249.6±37.2 b 469.7±18.1 ab – 1 229.5±73.7 a
Beni Fuji – 17.4±1.7 cd 12.5±0.4 cd 20.6±0.4 c – – – 33.2±4.7 de 12.8±0.5 d 30.3±0.6 f – 281.7±17.3 de 9.6±0.2 cd 418.2±23.6 e
Red Bharati 13.7±0.6 def 40.4±3.6 ab 11.0±1.0 d 9.2±2.4 e – 4.3±0.1 d – 16.5±0.6 ef 23.7±1.4 bc 143.1±7.6 b 212.1±12.8 b 362.7±45.0 cd 149.2±11.0 a 985.8±54.0 b
Summer Black 4.3±0.3 fg 18.3±2.5 cd – 12.4±1.9 de – 11.6±2.4 bc – 64.0±6.8 b 31.0±3.0 b 236.0±3.0 a 374.3±16.1 a 464.5±11.9 ab 172.6±3.3 a 1 388.9±8.8 a
Hutai-8 19.2±1.0 d 32.7±3.3 b – 41.9±1.2 a 9.2±0.2 c 8.8±0.2 c 3.4±0.1 a 39.4±9.2 cd 18.3±1.3 cd 92.4±1.1 cd 32.2±6.3 c 238.6±26.4 ef 74.2±16.5 b 610.4±71.0 d
Moldova 34.3±1.4 c 35.2±1.0 b – – 61.3±4.6 a 12.2±1.3 b – 28.4±5.5 de 30.6±3.8 b 123.6±1.5 bc 34.8±0.5 c 172.6±6.9 fg 95.2±0.5 b 628.2±15.8 d
Bound phenolics
Gold Finger 2.6±0.4 C 11.8±0.4 ABC 3.8±0.1 B – 10.3±2.8 CDEF – 1.3±0.1 E – – 5.0±0.3 B – 23.4±2.7 D – 58.3±0.0 FG
Hakuho 1.3±0.3 C 12.2±3.6 ABC 3.7±0.2 B – 8.4±0.2 DEFG – 0.7±0.1 E 24.8±1.3 C 4.9±0.4 DE 3.7±0.2 BCD 0.9±0.3 BC 14.1±1.6 E 0.3±0.1 BC 75.0±2.6 FG
White Olympia 0.8±0.1 C 14.5±0.2 AB 5.0±0.1 AB 5.6±0.4 A 11.2±0.1 CDE – 1.8±0.1 E 11.4±0.8 CD 7.2±0.3 D 3.0±0.1 BCD 1.0±0.6 BC 22.2±0.1 D – 83.7±1.0 DEFG
Shine Muscat 5.6±0.4 B 6.8±0.4 BCD 4.6±0.7 B – 11.5±0.6 BCD 1.9±0.1 D 1.6±0.5 E 11.5±1.3 CD 22.8±0.8 A 5.4±1.0 B 2.2±0.9 AB 4.4±1.1 F – 78.3±4.0 EFG
Kyoho 29.7±1.5 A 19.7±5.9 A 7.1±1.7 A 5.6±0.6 A 18.3±1.6 A 8.3±1.2 B 41.5±4.6 A 70.0±10.2 A 15.5±1.1 B 24.3±1.4 A – 5.5±0.3 F 2.7±0.2 A 248.0±27.3 A
Muscat Kyoho 2.2±0.0 C 4.3±0.1 CD 4.2±0.0 B 2.8±0.1 B 5.5±0.2 G 2.0±0.1 D 2.7±0.2 E 18.5±1.1 C 2.8±0.2 EF 2.0±0.1 CD – 3.8±0.7 F – 50.9±0.2 G
Beni Fuji 6.4±0.4 B 11.3±1.3 ABC – – 13.1±0.0 BC 5.1±0.3 C 23.2±0.5 C 42.3±0.6 B – 5.2±0.9 B – 70.3±3.0 A – 177.1±6.1 B
Red Bharati 2.6±0.1 C 7.4±1.0 BCD 4.4±0.2 B 4.9±0.6 A 7.2±0.3 FG 2.2±0.1 D 6.4±1.9 E 13.6±1.0 CD 10.6±1.9 C 4.5±1.2 BC 3.4±1.1 A 46.4±0.9 B 0.3±0.0 BC 114.0±2.0 CDE
Summer Black 0.8±0.1 C 4.2±0.3 CD – – 7.5±0.2 EFG 2.3±0.0 D 14.4±0.3 D 21.3±3.8 C – 1.8±0.0 CD – 40.9±1.8 B – 93.3±7.0 CDEF
Hutai-8 0.8±0.1 C – 7.0±0.3 A 2.9±0.2 B 11.6±0.1 BCD 5.5±0.6 C 28.1±0.1 C 49.0±2.6 B 7.0±0.7 D 1.2±0.1 D – 1.2±0.1 F 0.2±0.0 CD 114.4±4.5 CD
Moldova 6.2±0.6 B 6.4±2.2 BCD 4.7±0.0 B – 15.2±0.1 AB 10.9±0.4 A 34.5±0.3 B 14.4±1.5 C – 3.0±0.0 BCD – 31.8±0.4 C 0.6±0.0 B 127.5±5.6 C
1)
GA, gallic acid; CAT, caftaric acid; DHB, 3,4-dihydroxybenzoic acid; VA, vanillic acid; CAF, caffeic acid; SYA, syringic acid; p-CMA, p-coumaric acid; C, (+)-catechin; EC, (–)-epicatechin;
RT, rutin; IQE, isoquercitrin; KAE, kaempferol; RES, resveratrol.
Data are mean±SD (n=3). Values with different capital or lowercase letters in each column are significantly different (P<0.05). –, not found.

Moldova.
LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158

4. Discussion
differences (P<0.05).
(4.19 µmol TE g–1 FW).

by Kyoho, Red Bharati, Hutai-8 and

Moldova, Hutai-8 were the second

For pulps, the average ORAC values

was beneficial for human health.

In general, the ORAC of free

showed higher ORAC values than these

Kyoho had the highest ORAC value
For the free phenolics, the variety of
µmol TE g–1 FW for bound phenolics.

eaten. Our result showed that the most

pulp, but skins and seeds were seldom
the highest ORAC value. There were
Hutai-8 (12.47 µmol TE g–1 FW) had

grapes are commonly consumed with

Grapes were rich in phenolic acids and
Black, and others had no significant
ORAC value (9.62 µmol TE g–1 FW). For

flavonoids (Yilmaz et al. 2014). Fresh

vegetables rich in phenolic compounds
highest ORAC, subsequently followed

Consumption of fresh fruits and

(4.73 µmol TE g–1 FW), followed by Red
no significant differences in the ORAC
Hakuho (12.51 µmol TE g–1 FW) and
g–1 FW, and 1.50 µmol TE g–1 FW for
of the ORAC values of free phenolics
shown in Fig. 2, for skins, the average

in pulps. Muscat Kyoho showed the

The free and bound phenolics in skins
(P<0.05). For the bound phenolics,
Muscat Kyoho (16.24 µmol TE g–1 FW),
TE g–1 FW, 87.16 µmol TE g–1 FW), and
(103.33 µmol TE g–1 FW, 93.15 µmol
value (190.57 µmol TE g–1 FW); Kyoho,
Muscat Kyoho had the highest ORAC
was 72.13 µmol TE g–1 FW, and 10.44

of free phenolics was 10.18 µmol TE

g–1 FW); Gold Finger showed the lowest

phenolics were stronger than bound

Bharati, Muscat Kyoho and Summer
Shine Muscat presented the lowest

values of the rest eight grape pulps

bound phenolics. For the free phenolics,
the highest ORAC value (16.14 µmol TE

phenolics both in grape pulps and skins.

the bound phenolics, Beni Fuji presented
1153
Table 4 Contents of phenolic acids, selected flavonoids, and resveratrol of grape pulps (µg g–1 FW)1)
1154
Phenolic acids Flavonoids
Variety RES Total
GA CAT DHB VA CAF SYA p-CMA C EC RT IQE KAE
Free phenolics
Gold Finger 44.9±4.8 a 42.2±0.8 cde 5.9±0.6 b 2.9±0.3 a – 2.6±1.2 cd – 27.6±8.6 de 9.3±2.0 fg 5.8±1.2 ab 1.9±0.1 bcd 21.8±1.6 a – 165.0±17.9 b
Hakuho 5.3±0.4 b 85.6±2.5 bc 7.3±0.1 b 2.0±0.3 ab 4.4±0.6 b 3.9±0.8 bc – 45.1±1.2 cd 36.9±1.8 ab 8.5±0.2 a 3.0±0.3 bc 1.8±0.2 cd – 203.8±0.5 ab
White Olympia 43.1±0.5 a 32.2±3.7 de – 4.2±0.0 a – 4.0±0.3 bc – 55.8±0.5 bc 15.6±0.2 ef – – 5.8±0.2 b – 160.7±5.1 b
Shine Muscat 3.0±0.2 b 48.5±1.5 cde – – 4.8±0.0 b 1.4±0.0 de – 13.0±0.7 ef 4.4±0.2 g 5.7±0.7 ab 0.8±0.1 cd – – 81.6±1.6 c
Kyoho 2.3±0.2 b 68.6±0.3 bcd 6.0±0.0 b – 4.8±0.1 b 5.6±0.0 ab – 67.7±3.2 b 26.8±0.5 cd – – 5.2±0.5 bc – 187.0±3.2 ab
Muscat Kyoho 27.8±0.5 a 56.9±2.0 cde 12.2±3.0 a 3.5±0.7 a 4.8±0.7 b 2.8±0.5 cd 6.6±1.0 a 25.5±2.8 ef 45.5±6.3 a 4.1±2.0 ab 4.1±0.7 b 7.6±1.7 b – 201.2±6.0 ab
Beni Fuji 1.4±0.0 b 109.6±23.7 b – 3.9±0.2 a – 7.9±0.6 a – 61.8±5.7 bc 32.0±1.9 bc – – 5.4±1.2 b – 222.0±30.5 ab
Red Bharati 3.8±0.1 b 21.8±5.7 e – – – 5.7±0.5 ab – 134.5±1.2 a 18.8±0.8 de 6.3±0.9 a 10.1±0.9 a – – 201.0±7.9 ab
Summer Black 3.4±0.1 b 17.5±2.5 e – – 5.0±0.1 b 1.8±0.0 cde – 18.6±1.3 ef 19.1±0.7 de 6.0±0.8 a – 7.5±0.3 b 1.9±0.4 a 80.8±3.3 c
Hutai-8 7.5±3.3 b 192.3±28.0 a – 2.3±1.4 ab 7.0±0.1 a 1.8±0.1 cde – 8.3±0.2 f 27.4±2.2 cd – – 5.1±1.1 bc – 251.7±35.9 a
Moldova 4.8±0.7 b 12.4±5.6 e 6.5±0.5 b – 7.9±0.7 a – – 18.2±3.4 ef 6.5±0.1 g – – 1.8±0.2 cd 1.9±0.8 a 60.1±0.5 c
Bound phenolics
Gold Finger 1.2±0.4 B 2.9±0.1 BCD 1.7±0.1 B 1.0±0.1 C 2.8±0.0 C – – – – – – 2.4±0.0 BCD – 12.0±0.5 CDE
Hakuho 0.6±0.1 CD 1.5±0.2 CD 1.4±0.0 B 1.0±0.0 CD – – – – – – – 1.8±0.5 BCDE – 6.3±0.6 E
White Olympia – 5.8±0.1 B – 1.3±0.0 BC 2.1±0.1 D – – 5.5±0.6 B 1.6±0.3 B – – 0.8±0.1 EF – 17.2±1.2 C
Shine Muscat – – – 0.4±0.0 DE 2.8±0.2 C – – 1.4±0.0 D – – – 1.0±0.3 DEF – 5.7±0.1 E
Kyoho 1.0±0.1 BC 4.7±0.2 BC 2.8±0.0 A 1.6±0.0 B 3.7±0.2 B – 0.6±0.2 B 9.6±1.7 A 9.3±2.2 A – – 2.6±0.2 BC – 36.1±4.3 A
Muscat Kyoho 0.4±0.0 D 2.7±0.9 BCD – 0.9±0.1 CD 2.7±0.1 CD – – 1.9±0.5 CD – – – 3.2±0.3 AB – 11.8±1.8 CDE
Beni Fuji 0.4±0.1 D 9.2±0.6 A – 1.8±0.1 AB 4.7±0.1 A – 0.2±0.0 CD 4.9±0.2 B 1.0±0.0 B – – 2.4±0.3 BCD – 24.8±0.6 B
Red Bharati 1.8±0.1 A 4.6±0.8 BC 1.8±0.2 B 0.8±0.2 CD 3.0±0.1 C – 0.2±0.0 CD 9.8±0.4 A – – – 4.4±0.7 A – 26.5±0.8 B
Summer Black 0.1±0.0 D 2.9±0.3 BCD 1.8±0.5 B – 3.0±0.0 C 0.7±0.0 A 1.8±0.0 A 4.7±0.3 BC – – – – – 15.1±1.4 CD
Hutai-8 0.1±0.0 D 4.1±0.6 BC – 2.2±0.4 A 3.8±0.4 B – 0.2±0.0 CD 1.9±0.3 D – – – 1.4±0.2 CDEF – 13.6±1.6 CD
Moldova 0.3±0.0 D – 1.7±0.0 B 0.8±0.0 CD 2.7±0.0 C – 0.3±0.0 C 2.8±0.2 BCD – – – – – 8.7±0.3 DE
1)
GA, gallic acid; CAT, caftaric acid; DHB, 3,4-dihydroxybenzoic acid; VA, vanillic acid; CAF, caffeic acid; SYA, syringic acid; p-CMA, p-coumaric acid; C, (+)-catechin; EC, (–)-epicatechin;
RT, rutin; IQE, isoquercitrin; KAE, kaempferol; RES, resveratrol.
Data are mean±SD (n=3). Values with different capital or lowercase letters in each column are significantly different (P<0.05). –, not found.

(Fig. 4).
LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158

antioxidant activities.

dominant (Figs. 3-C and 4-C).

health benefits among the 11 grapes.

(–)-epicatechin, rutin, isoquercitrin

The phenolic compounds in skins and

abundant phenolics in grape skins were

Compared to other free phenolics in

free phenolics, free syringic acid and
showed the highest contents of total
antioxidant capacity. It means that
phenolic compounds, and the strongest

showed in Figs. 3-A and 4-A. Compared

result was in accordance with the reports

acids such as p-coumaric acid and

2015; Pantelić et al. 2016). Muscat

with p-coumaric acid, vanillic acid and

some free flavonoids: (+)-catechin,

in skins, Kyoho skin was characterized

and bound forms. For free phenolics
were identified using the loading plots
Pantelić et al. 2016). The contents of

pulps were different between the free

4-A). While for pulps, free phenolic
were the dominant (Figs. 3-A and
skins, free rutin, catechin, isoquercitrin,
The phenolic compounds of grapes
strongly depended on varieties, as
The phenolic compounds of grapes
variables responsible for the clustering
Muscat Kyoho may have the greatest
Kyoho had the highest content of total
(Yilmaz et al. 2014; Cosmulescu et al.
contents of phenolic compounds. This
and ORAC showed similar trend to the
previously (Pantelić et al. 2016). The
results were consistent with the report
were higher than in the pulps. These
reported before (Di Lecce et al. 2014;

3,4-dihydroxybenzoic acid were the

were different in skins and pulps.
and kaempferol, and the strongest
to other varieties, Muscat Kyoho
shown in Fig. 3, the main influential
The PCA correlation plots were
antioxidant activities assayed by DPPH
total phenolic contents in the skins
than the bound phenolics, and the

(–)-epicatechin, and kaempferol

free phenolics in grapes were higher
phenolic acids. Similar results were
flavonoids, and in grape pulps were
 LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158 1155

VC Free phenolics Bound phenolics

A B
60 60

50 A
50

EC50 values (μg mL–1)

EC50 values (μg mL–1)

B
40 A 40 D C
aE F F
B G
30 E D C E 30 H b
F F E I
G J
cd cd de c
20 aH b 20 g f g
e
f d de c c c e c h
g
10 10

0 0
Fi C
hi Ha er
Sh O uho

M pia

us K at
t K ho

R ni o
m ha ji

Bl i
H ck
M ai-8
va

Fi C
hi Ha er
Sh O uho

M pia

us K at
t K ho

R ni o
m ha ji

Bl i
H ck
M ai-8
va
er rat

er rat
Su d B Fu

Su d B Fu
Be oh

Be oh
V

V
c

c
ng

ng
a

a
do

do
ca yo

ca yo
in lym
us

in lym
us
te k

ut

te k

ut
ol

ol
d

d
e

e
m

m
ol

ol
e

e
G

G
M

M
W

W
Variety Variety

Fig. 1 The EC50 values of free and bound phenolics in skins (A) and pulps (B) of different grape varieties in the DPPH (1,1-diphenyl-
2-picrylhydrazyl) free radical scavenging experiments (mean±SD, n=3). Values with different capital or lowercase letters within
the same bar are significantly different at P<0.05.

Muscat Kyoho (skins) a D

Kyoho (skins) b B
Moldova (skins) bc AB
Hutai-8 (skins) bc D
Red Bharati (skins) c B
Summer Black (skins) d C
White Olympia (skins) de E
Hakuho (skins) ef F
Beni Fuji (skins) fg A
Gold Finger (skins) gh FG
Shine Muscat (skins) i E
Variety

0
Muscat Kyoho (pulp) hi HI
Hakuho (pulp) hi I
Hutai-8 (pulp) hi I
Kyoho (pulp) i F
Summer Black (pulp) i HI
Red Bharati (pulp) i GH
Beni Fuji (pulp) i I
Gold Finger (pulp) i I
Moldova (pulp) i I Free phenolics
White Olympia (pulp) i I Bound phenolics
Shine Muscat (pulp) i I

0 50 100 150 200

The ORAC values (μmol TE g–1 FW)

Fig. 2 The ORAC (oxygen radical absorbance capacity) values (µmol TE g–1 FW) of free and bound phenolics in grape skins and
pulps (mean±SD, n=3). Values with different capital or lowercase letters within the same bar are significantly different at P<0.05.

3,4-dihydroxybenzoic acid (Figs. 3-A and 4-A). For bound For bound phenolics in pulps, Kyoho pulp showed high
phenolics in skins, Kyoho skin was characterized with contents of catechin and (–)-epicatechin (Figs. 3-D and 4-D).
phenolic acids, catechin, rutin, and resveratrol (Figs. 3-B Correlations between the total phenolic contents and
and 4-B). For free phenolics in pulps, Kyoho pulp was antioxidant activities were analyzed, the results were shown
characterized with gallic acid and rutin (Figs. 3-C and 4-C). in Appendix B. There were significant correlations between
1156 LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158

A Variables/Loadings plot for data B Variables/Loadings plot for data

1.0 1.0
EC
CAF DHB
CAT IQE
0.5 RES 0.5 VA
PC2 (14.98%)

PC2 (20.08%)
EC RT CAT RT
DPPH
GA IQE SYA RES
FPC GA
0 0
ORAC CAF
C
C BPC
p-CMA
–0.5 DHB p-CMA
KAE
VA
–0.5 SYR
KAE DPPH ORAC

–1.0 –1.0
–1.0 –0.5 0 0.5 1.0 –1.0 –0.5 0 0.5 1.0
PC1 (42.63%) PC1 (44.64%)
C Variables/Loadings plot for data D Variables/Loadings plot for data
1.0 1.0
DHB p-CMA VA
CAF
ORAC CAT
0.5 EC 0.5
PC2 (19.08%)

PC2 (19.68%)
DPPH KAE
CAT
RES CAF
KAE DHB BPC
GA FPC
0 DPPH
0 ECC
RT GA
ORAC
IQE
–0.5 SYA
–0.5
C DHB
p-CMA

–1.0 –1.0
–1.0 –0.5 0 0.5 1.0 –1.0 –0.5 0 0.5 1.0
PC1 (30.98%) PC1 (41.26%)

Fig. 3 Loading plots of free and bound phenolics in grape skins (A and B, respectively) and pulps (C and D, respectively). FPC,
the total free phenolic contents determined by HPLC-DAD; BPC, the total bound phenolic contents determined by HPLC-DAD.
GA, gallic acid; CAT, caftaric acid; DHB, 3,4-dihydroxybenzoic acid; VA, vanillic acid; CAF, caffeic acid; SYA, syringic acid; p-CMA,
p-coumaric acid; C, (+)-catechin; EC, (–)-epicatechin; RT, rutin; IQE, isoquercitrin; KAE, kaempferol; RES, resveratrol; DPPH, the
EC50 values of DPPH free radical scavening assays; ORAC, the oxygen radical absorbance capacity values.

A Samples/Scores plot of data B Samples/Scores plot of data

2.0 Moldova
2.0

White Olympia Shine Muscat

1.0 1.0
PC2 (14.98%)

PC2 (20.08%)

Red Bharati Hakuho

Summer Black Kyoho
White Olympia
Gold Finger Muscat Kyoho Red Bharati
0 0 Gold Finger
Hutai-8
Hakuho Muscat Kyoho
Shine Muscat Hutai-8

–1.0 Beni Fuji –1.0 Moldova

Summer Black
Kyoho Beni Fuji

–2.0 –2.0
–3.0 –2.0 –1.0 0 1.0 2.0 3.0 –3.0 –2.0 –1.0 0 1.0 2.0 3.0
PC1 (42.63%) PC1 (44.64%)
C Samples/Scores plot of data D Samples/Scores plot of data
2.0 Muscat Kyoho
2.0
Beni Fuji
Hutai-8
1.0 Hutai-8 1.0
PC2 (19.08%)

PC2 (19.68%)

Muscat Kyoho
Moldova Hakuho
White Olympia
Summer Black Gold Finger
Kyoho
0 0 Shine Muscat
Gold Finger White Olympia Kyoho
Red Bharati
Shine Muscat Hakuho Beni Fuji
–1.0 –1.0 Moldova

Red Bharati
Summer Black
–2.0 –2.0
–3.0 –2.0 –1.0 0 1.0 2.0 3.0 –3.0 –2.0 –1.0 0 1.0 2.0 3.0
PC1 (30.98%) PC1 (41.26%)

Fig. 4 Principal component scores plots of free and bound phenolics in grape skins (A and B, respectively) and pulps (C and D,
respectively).

the contents of phenolics determined by HPLC-DAD and contents and ORAC values in pulps (P<0.01). There was
the ORAC values in skins (P<0.05), the bound phenolic no significant linear correlation between DPPH and ORAC
 LI Fu-xiang et al. Journal of Integrative Agriculture 2019, 18(5): 1148–1158
values except for the free phenolics in skins (P>0.05).
In general, the phenolic compounds of grapes strongly
depended on grape varieties and positions (skins and
pulps), and free and bound forms. There were strongly
linear correlation between the total phenolic contents and
antioxidant activities.
5. Conclusion
Fresh grape is rich of bioactive phenolic compounds. The
phenolic compounds of grapes strongly depend on grape
varieties. Muscat Kyoho has the most abundant phenolics
and the strongest antioxidant capacity. The phenolic
compounds of grapes are mainly in skins. Flavonoids are
the most abundant phenolics in skins, and phenolic acids
are the most abundant in pulps.
Acknowledgements
This work was supported by the National Key R&D Program
of China (2016YFD0400203) and the National Natural
Science Foundation of China (31471576).
Appendices associated with this paper can be available on
http://www.ChinaAgriSci.com/V2/En/appendix.htm
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Executive Editor-in-Chief WANG Qiang
Managing editor WENG Ling-yun