Accepted Manuscript Phenolic compositions and antioxidant capacities of Chinese wild mandarin (Citrus reticulata Blanco) fruits Yuanmei Zhang, Yujing Sun, Wanpeng Xi, Yan Shen, Liping Qiao, Liezhou Zhong, Xingqian Ye, Zhiqin Zhou PII: DOI: Reference:
S0308-8146(13)01081-9 http://dx.doi.org/10.1016/j.foodchem.2013.08.012 FOCH 14497
To appear in:
Food Chemistry
Received Date: Revised Date: Accepted Date:
31 January 2013 20 July 2013 2 August 2013
Please cite this article as: Zhang, Y., Sun, Y., Xi, W., Shen, Y., Qiao, L., Zhong, L., Ye, X., Zhou, Z., Phenolic compositions and antioxidant capacities of Chinese wild mandarin (Citrus reticulata Blanco) fruits, Food Chemistry (2013), doi: http://dx.doi.org/10.1016/j.foodchem.2013.08.012
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1
Phenolic compositions and antioxidant capacities of Chinese wild
2
mandarin (Citrus reticulata Blanco) fruits
3
Yuanmei Zhang
4
Xingqian Ye b*, Zhiqin Zhou a,c*
5
a
6
Chongqing 400716, China
7
b
8
Food science, Zhejiang University, Zhejiang Province, Hangzhou 310029, China
9
c
10
a,b
, Yujing Sun b, Wanpeng Xi
a,c
, Yan Shen b, Liping Qiao b, Liezhou Zhong b,
College of Horticulture and Landscape Architecture, Southwest University,
Department of Food Science and Nutrition, School of Biosystems Engineering and
Key Laboratory of Horticulture Science for Southern Mountainous Regions,
Ministry of Education, Chongqing 400715, China
11 12
*
13
[email protected] (Z. Zhou); Tel.: +86 571 88982155, fax: +86 571
14
88982550, e-mail:
[email protected] (X. Ye).
Corresponding author: Tel.: +86 23 68250229, fax: +86 23 68251274, e-mail:
15
1
16
Abstract
17
As one of the most important centers of origin for the genus Citrus L., China is rich
18
in wild mandarin germplasm. In this study, phenolic compounds in the peels of 14
19
wild mandarin genotypes native to China were determined and their antioxidant
20
capacities were evaluated using DPPH, FRAP, ABTS and ORAC methods. We found
21
that Nieduyeju had the highest total phenol content (51.14 mg/g DW), and
22
Wulongsuanju had the highest total flavonoid content (20.66 mg/g DW). Hesperidin,
23
the dominant flavonoid, was observed to be highest in Guangxihongpisuanju (55.98
24
mg/g DW). Ferulic acid was the most abundant phenolic acid analyzed, and
25
Nieduyeju (7780.17μg/g DW) and Guangxihongpisuanju (13607.19 μg/g DW) had
26
the highest contents of extractable and bound phenolic acid, respectively.
27
Antioxidant potency composite (APC) index showed obvious variations ranging
28
from 58.84 to 98.89 in the studied wild mandarins, among them, Nieduyeju had the
29
highest APC index. Overall, Guangxihongpisuanju, Nieduyeju, Cupigoushigan and
30
Daoxianyeju contained more phenolics and exhibited higher antioxidant capacities
31
than the mandarin cultivars Satsuma and Ponkan.
32 33 34
Keywords: Wild mandarins; Total phenolics; Flavonoid; Phenolic acid; Antioxidant
35
capacities
2
36
1. Introduction
37
Plant polyphenols are a large group of secondary metabolites that have important
38
functions in combating chronic diseases, such as type 2 diabetes, heart disease and
39
various cancers, because of their high antioxidant activities (Chavez-Santoscoy,
40
Gutierrez-Uribe, & Serna-Saldivar, 2009; Jiang & Dusting, 2003; Oboh & Ademosun,
41
2012). Citrus is one of the most important horticultural crops worldwide and their
42
fruits are abundant in phenolic compounds. Methanol extracts of citrus peels are rich
43
in flavones and glycosylated flavanones, while hydrolyzed extracts of citrus peels are
44
rich in flavonols and phenolic acids (Bocco, Cuvelier, Richard, & Berset, 1998).
45
Citrus fruit juices contain flavanones and phenolic acids (Rapisarda et al., 1999).
46
Many studies have focused on the quantification of phenolic compounds and
47
antioxidant capacity of citrus fruits such as lime, grapefruits, sweet orange, lemon,
48
and tangerine (Abad-Garcia, Garmon-Lobato, Berrueta, Gallo, & Vicente, 2012;
49
Goulas & Manganaris, 2012; Kelebek, Canbas, & Selli, 2008). However, only a few
50
studies have sought to determine the phenolic compounds and antioxidant activity of
51
wild citrus fruits, especially wild mandarin fruits.
52
China is the most important center of origin for the genus Citrus L., and some
53
important wild citrus species or variety originated from the country. Over the past few
54
decades, many wild mandarin genotypes native to China have been described, such as
55
Citrus. mangshanensis S. W. He & G. F. Liu and C. daoxianensis S. W. He & G. F.
56
Liu (Liu & Deng, 2007). Thus far, several researchers have investigated the
57
phylogeny of these wild mandarins using nuclear and chloroplast simple sequence 3
58
repeat markers, nuclear LEAFY second intron and plastid trnL-trnF sequences, and
59
random amplified polymorphic DNA (RAPD) (Leng et al., 2012; Li, Cheng, Guo, Xu,
60
& Deng, 2006; Li, Cheng, Tao, & Deng, 2007). However, the phenolic compounds
61
and antioxidant activity of wild mandarins have rarely been studied.
62
The objective of the present study is to determine the content and composition of
63
phenolic compounds in 14 Chinese wild mandarin genotypes and evaluate their
64
antioxidant capacity. The results obtained were compared with those of the mandarin
65
cultivars ‘Satsuma’ and ‘Ponkan’, the most commonly cultivated mandarin fruits
66
types, to provide useful information for future utilization of Citrus germplasm.
4
67
2. Materials and methods
68
2.1. Chemicals
69
Eriocitrin, taxifolin, narirutin, neohesperidin, rhoifolin, quercitrin, eridictyol, didymin,
70
poncirin, naringenin, luteolin, kaempferol, diosmetin, sinensetin, nobiletin, tangeretin,
71
protocatechuic acid, p-hydroxybenzoic acid, vanillic acid, caffeic acid, p-coumaric
72
acid, ferulic acid, sinapic acid, chlorogenic acid, Folin–Ciocalteu phenol reagent,
73
2,2-diphenyl-1-picrylhydrazyl
74
2,2′-azino-bis(3-ethylbenzthiozoline-6)-sulphonic
75
(2-pyridyl)-S-triazine
76
dihydrochloride (AAPH), trolox (6-hydrox-2,5,7,8-tetramethylchromane-2-carboxylic
77
acid) and fluorescein were purchased from Sigma (St. Louis, MO, USA). Naringin
78
and hesperidin were obtained from the National Institutes for Food and Drug Control
79
(Beijing, China). The methanol of high-performance liquid chromatography (HPLC)
80
grade was purchased from Merck KgaA (Darmstadt, Germany). All the other reagents
81
of analytical grade were bought from Sinopharm Chemical Reagent Co., Ltd.
82
(Shanghai, China).
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2.2. Fruit materials
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All citrus fruits were collected from the National Citrus Germplasm Repository,
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Citrus Research Institute of Chinese Academy of Agricultural Sciences, Chongqing,
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China (Table 3). Fruits were harvested at commercial maturity stage based on external
87
colour and size uniformity. After harvest, pooled peel samples of each genotype were
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freeze-dried, ground, and sieved through a 40-mesh sieve. The powders were stored at
(TPTZ),
radicals
2,2´-
5
acid
azobis
(DPPH), (ABTS),
2,4,6-tris
(2-methylpropionamidine)
89
–80 °C until analysis.
90
2.3. Sample extraction
91
The extraction procedure was based on the method of Ramful, Tarnus, Aruoma,
92
Bourdon, and Bahorun (2011) with some modifications. Methanol (80%, 24 mL) was
93
added to 1 g of lyophilized powder samples. The mixture was shaken for 12 h and
94
centrifuged at 3000 g for 10 min at 4 °C. Methanol (80%, 24 mL) was added to the
95
residue and the same procedure was repeated. Supernatants from both extractions
96
were collected and diluted to 50 mL with methanol. The solutions were then stored at
97
–20 °C for determination of total phenol, total flavonoid, extractable phenolic acids,
98
and antioxidant activity. The residue was further used to determine bound phenolic
99
acids using the method of Ye et al. (2011).
100 101
2.4. Determination of total phenolic content, total flavonoid content, and antioxidant capacity
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Total phenolic content was determined using the Folin-Ciocalteu method (Xu et al.,
103
2008). The total flavonoid content was determined using the method of Wang,
104
Chuang, and Hsu (2008). DPPH, ABTS, ferric reducing ability of plasma (FRAP) and
105
oxygen radical antioxidant capacity (ORAC) assays were used to evaluate the
106
antioxidant capacity (Almeida et al., 2011; Rapisarda, Fabroni, Peterek, Russo, &
107
Mock, 2009; Xu et al., 2008).
108
2.5. Analysis of phenolic acids by HPLC
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Phenolic acid contents, including both extractable and bound phenolic acids, were
110
determined using the method of Ye et al. (2011). The HPLC condition was followed 6
111
as described by Xu et al. (2008).
112
2.6.Analysis of flavonoids by HPLC
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About 0.5 g of freeze-dried sample powder was extracted with methanol (80%, 12 mL)
114
and dimethyl sulphoxide (1:1, v/v) following the procedures described in Section 2.3.
115
The flavonoids contents were determined by HPLC method as described in our
116
previous report (Zhang et al., 2012). After filtration on Millipore membrane (0.22 µm),
117
10 µL of the solution was injected into the HPLC system. Chromatographic
118
separation was performed using a reverse phase column (ZORABX SB-C18, 250
119
mm×4.6 mm internal diameter). The mobile phase was composed of (A) 0.1% formic
120
acid (aqueous) and (B) methanol. Gradient elution was performed as follows: from
121
0-20 min, 37-50% B; from 20-35 min, 50-80% B; from 35-40 min, 80-100% B; from
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40-50 min, 100% B; from 50-60 min, 37-50% B. The column temperature was
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maintained at 25 °C and the flow rate was 0.7 mL/min. Flavanones, flavones and
124
flavonols were detected at wavelengths of 283, 330 and 367 nm, respectively.
125
2.7. Statistical analysis
126
All data are expressed as the means ± standard deviation of three replicates. Statistical
127
analysis was performed using SPSS v19.0 software (SPSS for Windows, Release 19.0,
128
SPSS Inc.). Significant differences among the samples were calculated using one-way
129
ANOVA, followed by Duncan’s multiple-range test at 5% level (p ≤ 0.05).
7
130
3. Results and discussion
131
3.1. Flavonoid contents
132
In the present study, a total of 18 flavonoids were identified, including 10 flavanones,
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seven flavones and one flavonol compounds (Table 1). We found that the variation
134
patterns of flavonoid components and contents were largely the same for the different
135
genotypes studied (Fig. 1). This result provides direct evidence that phenolic
136
compounds are genetically controlled.
137
Flavanones were the major flavonoids of the wild mandarins tested, and
138
hesperidin was the major flavanone, followed by narirutin and eriocitrin. The contents
139
of these flavanones varied from not detected (ND) to 55.98 mg/g dry weight (DW),
140
ND to 6.89 mg/g DW, and 0.79 to 8.51 mg/g DW, respectively. Guangxihongpisuanju
141
had the highest content of hesperidin, and Cupigoushigan the highest narirutin and
142
eriocitrin contents. Guangxihongpisuanju had a higher hesperidin content than the
143
cultivars Satsuma and Ponkan. The eriocitrin contents of Cupigoushigan, Daoxianyeju
144
and Nieduyeju were 4.2 to 10.91 times higher than those of the cultivars Satsuma and
145
Ponkan.
146
In general, mandarin fruits have a distinct flavanone profile that is dominated by
147
hesperidin and narirutin (Peterson et al., 2006), and this is largely confirmed by our
148
results. Instead of hesperidin and narirutin, however, naringin and neohesperidin were
149
found to be dominant in Xichuanzhoupigan and Wangcangzhoupigan. The peels of
150
them contained approximately 4 times more naringin and 10 times more
151
neohesperidin than the rest of materials studied. These results suggested that 8
152
Xichuanzhoupigan and Wangcangzhoupigan may be excellent sources of naringin and
153
neohesperidin.
154
Among the seven flavones identified in this study, nobiletin was the most
155
abundant flavone composition, followed by tangeretin and sinensetin (Table 1). The
156
contents of these flavones varied from 2.25 to 6.83 mg/g DW, 0.87 to 2.92 mg/g DW,
157
and 0.12 to 4.71 mg/g DW in the wild materials, respectively. Wulongsuanju and
158
Nieduyeju had the highest levels of nobiletin and sinensetin, repectively, while
159
Banyeshengjuzi No.2 had the highest tangeretin content. The nobiletin content of
160
Wulongsuanju was 1.05- to 13.40- fold higher than those of the cultivars Satsuma and
161
Ponkan. The sinensetin contents of Nieduyeju, Cupigoushigan and Daoxianyeju were
162
3.98- to 67.29- fold higher than those of the cultivars Satsuma and Ponkan.
163
Kaemperol was only found in four genotypes, namely, Daoxianyeju, Nieduyeju,
164
Cupigoushigan and Jizigan.
165
Lu, Zhang, Bucheli, and Wei (2006) found that Zaoju (C. subcompressa Tanaka)
166
has the highest nobiletin content (5.9 mg/g DW) among 13 citrus species, while
167
Gongju (C. kinokuni hort. ex. Tanaka), Yongchunlugan (C. reticulata Blanco) and
168
Hamlin (C. sinensis Osbeck) has the highest sinensetin contents (0.5 mg/g DW) in the
169
citrus species analyzed. Bermejo, Llosa, and Cano (2011) found that the nobiletin,
170
tangeretin and sinensetin contents in the peels of mandarin fruits ranged from 0.45 to
171
0.61 mg/g DW, 0.27 to 0.86 mg/g DW, and 0.12 to 0.25 mg/g DW, respectively. In
172
this study, we found that the nobiletin contents of Wulongsuanju and Jizigan were
173
higher than those reported by Lu et al. (2006). We also noticed that the nobiletin and 9
174
tangeretin contents of our wild mandarin fruits were higher than those reported by
175
Bermejo et al. (2011). Moreover, the sinensetin contents in most of the wild mandarin
176
peels, especially in those of Nieduyeju, Cupigoushigan, Daoxianyeju and
177
Wulongsuanju, were much higher than those reported in current literatures (Bermejo
178
et al., 2011; Lu et al., 2006).
179
3.2. Phenolic acid content
180
The extractable and bound form phenolic acids, including hydroxybenzoic acid,
181
hydroxycinnamic acid and chlorogenic acid of the 14 wild mandarin genotypes were
182
determined and the results were shown in Table 2 and Fig. 2. Ferulic acid was the
183
most dominant extractable phenolic acid, followed by caffeic acid, p-coumaric acid
184
and sinapic acid. The contents of these extractable phenolic acids varied from 1730.93
185
to 7780.17 μg/g DW, 96.53 to 1256.20 μg/g DW, 198.66 to 834.77 μg/g DW, and ND
186
to 342.84 μg/g DW in the tested materials, respectively. Nieduyeju had the highest
187
ferulic acid content, while Guangxihongpisuanju had the highest caffeic acid and
188
p-coumaric acid contents. Dakengyeju had the highest sinapic acid content. Overall,
189
Nieduyeju,
190
Banyeshengjuzi No.1 had higher ferulic acid contents than those of the cultivars
191
Satsuma and Ponkan.
Dakengyeju,
Guangxihongpisuanju,
Jinju,
Xipigoushigan
and
192
The ferulic acid was also the most dominant bound phenolic acid, followed by
193
p-coumaric acid and caffeic acid. Guangxihongpisuanju had the highest contents of
194
ferulic acid, p-coumaric acid and caffeic acid, while Wangcangzhoupigan had the
195
lowest ferulic acid and caffeic acid contents. Most of the wild mandarin genotypes 10
196
tested had a higher ferulic acid content than the cultivars Satsuma and Ponkan. In
197
particular, the ferulic acid content of Guangxihongpisuanju was 3-fold higher than
198
those of the cultivars Satsuma and Ponkan. In addition, Guangxihongpisuanju had
199
higher p-coumaric acid and caffeic acid contents than the cultivars Satsuma and
200
Ponkan.
201
Bocco et al. (1998) found that ferulic acid is the main phenolic acid in citrus
202
fruits, and the abundance of hydroxycinnamic acids in citrus varied in the following
203
order: ferulic acid (0.036–1.580 mg/g DW) > sinapic acid (0.030–0.954 mg/g DW) >
204
p-coumaric acid (0.071–0.193 mg/g DW) > caffeic acid (0.006–0.229 mg/g DW).
205
Wang et al. (2008), however, reported that chlorogenic acid rather than ferulic acid is
206
the main phenolic acid in the peels of citrus fruits, and the contents of phenolic acids
207
varied as the following order: chlorogenic acid (145–339 μg/g DW) > p-coumaric
208
acid (41.7–346 μg/g DW) > ferulic acid (30.3–150 μg/g DW) > sinapic acid
209
(10.1–178 μg/g DW) > caffeic acid (3.06–80.0 μg/g DW). Our results showed that
210
ferulic acid is the most abundant phenolic acid in the peels of the wild mandarins
211
tested, similar to the results obtained by Bocco et al. (1998). However, the variation
212
order of the hydroxycinnamic acid contents observed in our study was different as
213
follows: ferulic acid > p-coumaric acid and caffeic acid > sinapic acid. It is
214
noteworthy that the contents of ferulic acid, p-coumaric acid, caffeic acid and sinapic
215
acid of the wild mandarins tested in this study were all higher than those reported by
216
previous studies. The chlorogenic acid content, however, was lower than that obtained
217
by Wang et al. (2008). These differences may be attributed to the genetic backgrounds 11
218
of the citrus species and /or environmental factors.
219
3.3. Total phenolic content, total flavonoid content and antioxidant capacities
220
The total phenolic contents of methanol extracts from the peels of 14 wild mandarin
221
genotypes and two cultivars were measured. Their antioxidant capacities were
222
evaluated by DPPH, FRAP, ABTS, and ORAC methods. The total phenolic contents
223
showed obvious variations among the different genotypes ranging from 29.38 to
224
51.14 mg/g DW (gallic acid equivalents) (Table 3). This variation range is higher than
225
that (15.595 to 18.950 mg gallic acid equivalents/g DW) of ethanol extracts of C.
226
reticulata Blanco cv. Ougan fruits (Chen, Yuan, & Liu, 2010), but lower than that
227
(104.2 to 172.1 mg gallic acid equivalents/g DW) of extracts of C. reticulata Blanco
228
fruits (Ghasemi, Ghasemi, & Ebrahimzadeh, 2009). Nieduyeju had the highest total
229
phenolic content, followed by Dakengyeju, Cupigoushigan and Daoxianyeju.
230
Wulongsuanju had the lowest total phenolic content. In addition, we found that the
231
total phenolic contents of Nieduyeju, Dakengyeju, Cupigoushigan, Daoxianyeju,
232
Xipigoushigan and Banyeshengjuzi No.2 were all higher than those of the cultivars
233
Satsuma and Ponkan.
234
The total flavonoid contents differed significantly (p < 0.05) among the wild
235
mandarin genotypes tested. The total flavonoid contents varied from 7.95 to 20.66
236
mg/g DW (rutin equivalents) (Table 3). These data are partially in accordance with the
237
results (0.3 to 31.1mg quercetin equivalents/g DW) reported by Ghasemi et al. (2009),
238
but much higher than those (4.671 to 5.796 mg rutin equivalents/g DW) obtained by
239
Chen et al. (2010). The highest total flavonoid content (20.66 mg/g DW) was found in 12
240
Wulongsuanju, and it is significantly different (p < 0.05) from other wild genotypes
241
tested. No significant differences (p > 0.05) were observed between the total
242
flavonoid contents of Daoxianyeju and Nieduyeju, and they ranked second in term of
243
the total flavonoid content among all the genotypes studied. The total flavonoid
244
contents of Guangxihongpisuanju and Jizigan were more or less the same, and they
245
ranked third among all the genotypes studied. It is noteworthy that the total flavonoid
246
contents of Wulongsuanju, Nieduyeju, Daoxianyeju, Jizigan, Guangxihongpisuanju
247
and Cupigoushigan were all higher than those of the cultivars Satsuma and Ponkan.
248
The DPPH assay has been widely used for the determination of primary
249
antioxidant capacity. DPPH radical could be decreased by reactions with antioxidant
250
compositions that can donate hydrogen (Kumaran & Joel Karunakaran, 2007). The
251
DPPH values of the wild mandarins varied from 29.04 to 50.46 μmol trolox
252
equivalents (TE)/g DW. Cupigoushigan and Nieduyeju had the highest DPPH values
253
and no significant difference was observed between them (p > 0.05). On the other
254
hand, Tuju had the lowest DPPH value. Six out of 14 wild mandarins tested, including
255
Cupigoushigan,
256
Daoxianyeju, had higher DPPH values than those of the cultivars Satsuma and
257
Ponkan.
Nieduyeju,
Dakengyeju,
Jinju,
Guangxihongpisuanju
and
258
The FRAP method is commonly applied to determine the antioxidant activity of
259
plant materials, and it measures the capacity of the sample to reduce ferric complex to
260
the ferrous form (Contreras-Calderón, Calderón-Jaimes, Guerra-Hernández, &
261
García-Villanova, 2011). The FRAP values of the 14 wild mandarins analyzed ranged 13
262
from 26.50 to 46.98 μmol TE/g DW. The highest FRAP value was found in Nieduyeju,
263
whereas the lowest FRAP value was found in Wulongsuanju. Six out of 14 wild
264
mandarins tested, including Nieduyeju, Cupigoushigan, Daoxianyeju, Dakengyeju,
265
Jinju and Xipigoushigan, had higher FRAP values than those of the cultivars Satsuma
266
and Ponkan.
267
The ABTS method is also commonly used to study the antioxidant capacity of
268
plants based on the capacity to scavenge the radical cation ABTS+• generated in the
269
system (Kim, Lee, Lee, & Lee, 2002). The ABTS values of the 14 wild mandarins
270
analyzed ranged from 65.62 to 108.60 μmol TE/g DW. The highest ABTS value was
271
found in Nieduyeju, whereas the lowest ABTS value was found in Wulongsuanju.
272
Seven out of 14 wild mandarins tested, including Nieduyeju, Banyeshengjuzi No.1,
273
Banyeshengjuzi No.2, Dakengyeju, Xipigoushigan, Jinju, and Daoxianyeju, had
274
higher ABTS values than those of the cultivars Satsuma and Ponkan.
275
The ORAC assay has found broader application for determining the antioxidant
276
capacity of botanical and biological samples (Prior et al., 2003; Rapisarda, Fabroni,
277
Peterek, Russo, & Mock, 2009). This method is based on a hydrogen atom transfer
278
reaction mechanism, which is most relevant to human biology (Prior et al., 2003). The
279
ORAC values of the 14 wild mandarins tested ranged from 395.66 to 834.37 μmol
280
TE/g DW. The highest ORAC value was found in Nieduyeju, whereas the lowest
281
ORAC value was found in Jizigan. Among the 14 wild mandarins tested, only
282
Nieduyeju had a higher ORAC value than those of the cultivars Satsuma and Ponkan.
283
Given that the four methods used above resulted in different antioxidant 14
284
capacities for the same genotypes, an overall antioxidant potency composite (APC)
285
index was calculated for each genotype using the method described by Seeram et al.
286
(2008). The resulting APC indices are shown in Table 3. The APC index of different
287
mandarins showed obvious variation ranging from 58.84 to 98.89. Nieduyeju had the
288
highest APC index, followed by Cupigoushigan, Dakengyeju and Daoxianyeju.
289
Wulongsuanju had the lowest APC index.
290
Phenolic compounds, including flavonoids and phenolic acids, are known to be
291
responsible for antioxidant activity in fruits. Fruits with higher total phenolic content
292
generally showed stronger antioxidant capacity (Rice-Evans & Miller, 1996). The
293
high antioxidant activity of Nieduyeju, Cupigoushigan, Dakengyeju, and Daoxianyeju
294
may be attributed to their phenolic compositions and contents.
15
295
4. Conclusions
296
The phenolic compositions and antioxidant capacities of the Chinese wild mandarins
297
are reported for the first time in the present study. Significant variations in total
298
phenol and total flavonoid contents were observed in the 14 genotypes studied. We
299
found that the wild mandarin fruits were rich in polyphenols. A total of 18 flavonoids
300
and eight phenolic acids were identified from the genotypes studied. Among the
301
compounds identified, hesperidin, narirutin, eriocitrin, nobiletin and ferulic acid were
302
found to be the major phenolic compounds. Among the 14 wild mandarins tested,
303
Nieduyeju and Wulongsuanju had the highest total phenolic and total flavonoid
304
contents, respectively. Nieduyeju had the highest ferulic acid content of the
305
extractable phenolic acid, while Guangxihongpisuanju had the highest ferulic acid
306
content of the bound phenolic acids. The eriocitrin levels of Nieduyeju,
307
Cupigoushigan, and Daoxianyeju were 4- to 10- fold higher than those of the cultivars
308
Satsuma and Ponkan. Wulongsuanju had 1- to 13-fold higher nobiletin content than
309
the cultivars Satsuma and Ponkan. Guangxihongpisuanju had the highest hesperidin
310
content. The APC index also showed obvious variation ranging from 58.84 to 98.89 in
311
the wild mandarins studied, among them, Nieduyeju had the highest APC index. In a
312
word, our findings provide useful information for future study and utilization of the
313
wild mandarin germplasm in China and abroad.
314
16
315
Acknowledgements
316
This work was supported by the National Natural Science Foundation of China (Nos.
317
31171930, 31071635), the Fundamental Research Funds for the Central Universities
318
(XDJK2013A014), the Program for Chongqing Innovation Team of University
319
(KJTD201333), and the ‘111’ Project (B12006).
320
17
321
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322
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425
Figure captions:
426
Fig. 1. Variations pattern of flavonoid components and contents in the peel extracts of
427
the 14 wild mandarin genotypes and two cultivars analyzed in this study.
428
Fig. 2. Variations pattern of phenolic acid components and contents in the peel
429
extracts of the 14 wild mandarin genotypes and two cultivars analyzed in this study.
430
(A) Extractable phenolic acids, (B) bound phenolic acids.
22
Table 1 The flavonoid contents in the peels of the 14 wild mandarin genotypes and 2 cultivars analyzed in this study (mg/g DWa)b. Genotypes
Flavanone Eriocitrin
Taxifolin
Narirutin
Neohesperidin
Eridictyol
Didymin
Poncirin
20.39±0.23g
0.21±0.04c
0.07±0.00f
0.84±0.02j
0.14±0.04ij
28.41±0.89
d
0.87±0.01
b
0.12±0.01
c
1.58±0.04
g
0.17±0.02
ij
20.38±0.46
g
0.22±0.01
c
0.13±0.00
b
2.28±0.01
d
0.50±0.02
fg
26.42±0.90
e
0.15±0.01
c
1.10±0.06
hi
0.37±0.01
gh
29.52±0.68
d
0.89±0.04
b
2.52±0.01
c
1.58±0.06
c
55.98±1.23
a
1.84±0.02
f
0.83±0.02
e
18.23±0.51
h
ij
0.28±0.01
hi
Naringenin
Rhoifolin
ND
0.82±0.13f
Quercitrin
Luteolin
0.86±0.21a
0.09±0.01efg
Diosmetin
Sinensetin
Nobiletin
0.06±0.02f
0.15±0.06ij
4.10±0.18ef
0.35±0.01
b
3.54±0.06
c
3.02±0.09
g
0.11±0.00
de
4.71±0.29
a
4.29±0.23
de
0.94±0.10
f
5.46±0.29
c
0.56±0.01
gh
5.43±0.02
c
0.23±0.01
ij
2.74±0.07
g
h
4.51±0.08
d
0.79±0.20j
DX
7.75±0.35
b
7.72±0.27
c
1.35±0.01
ij
1.12±0.11
j
3.43±0.05
d
TG
1.03±0.08
j
ND
ND
0.98±0.03
ND
ND
0.49±0.00
WL
2.90±0.47def
0.81±0.23b
3.44±0.59e
0.48±0.11d
29.39±0.54d
ND
ND
0.66±0.09k
ND
ND
0.58±0.16g
ND
0.08±0.01fg
ND
2.15±0.27d
JJ
2.77±0.14ef
0.50±0.08cd
3.44±0.16e
ND
33.30±0.57c
ND
ND
1.09±0.23hi
0.54±0.01f
0.12±0.01de
1.41±0.01d
0.30±0.01b
0.10±0.01efg
ND
CP
8.51±0.13a
0.37±0.01de
6.89±0.13b
ND
24.93±0.63f
0.63±0.01bc
ND
3.79±0.00a
1.37±0.01d
0.49±0.01a
0.93±0.02ef
ND
0.12±0.01def
XP
2.66±0.07efg
ND
3.54±0.08e
ND
17.53±1.01h
0.74±0.00bc
ND
0.51±0.03k
0.48±0.02fg
0.47±0.03a
3.94±0.01a
ND
0.45±0.02a
ND
d
ND
1.17±0.02
h
0.25±0.04
l
BY No.1 BY No.2 GX
JZ XC WC
2.13±0.08
gh
2.59±0.20
fg
3.21±.59
de
0.78±0.00
j
PK
1.84±0.09
hi
Total
50.04
ST
0.34±0.02
def
ND 0.49±0.01
cd
1.35±0.06
a
ND 0.16±0.01
fg
0.66±0.01
bc
0.25±0.06
ef
ND
6.60±0.91
b
5.83±0.18
c
1.49±0.04
g
4.01±0.15
e
5.09±0.06
d
1.16±0.01
g
2.66±0.02
f
1.52±0.02
g
ND 1.35±0.11
0.06±0.01 0.27±0.01
ef
13.61±0.32 2.34±0.15 62.85
f
c
ND
ND g
5.46
1.28±0.26g
Hesperidin
Flavonol
DK
ND
0.51±0.10cd
Naringin
Flavone
a
0.12±0.01
d
2.78±0.15
b
0.56±0.01
d
0.04±0.00
d
29.37±0.33
4.54±0.05
a
4.28±0.92
a
0.75±0.01
i
ND 36.18±0.81
b
ND
33.29±0.39
c
14.13
404.05
ND
ND
ND
0.24±0.00
c
11.27±0.55
a
11.69±0.46
a
ND
0.46±0.01
a
0.09±0.01
e
ND ND ND
ND 2.82±0.05
b
e
ND
ND
2.01±0.03
26.9
0.86
23.41
0.92±0.01
e
2.26±0.12
a
2.02±0.19
b
0.06±0.00
j
0.92±0.01
e
12.41
ND 0.07±0.00
ef
0.05±0.01
f
0.37±0.05
b
0.15±0.05
d
0.05±0.01
f
0.10±0.00
def
0.25±0.02
c
0.25±0.03
c
ND 0.12±0.01 2.47
ND, not detectable. a Data are expressed as means ± standard deviation of triplicate samples. b Different superscripts between rows represent significant differences between samples (p < 0.05).
de
1.87±0.02
bc
0.74±0.01
fg
2.09±0.37
b
1.80±0.03
c
1.09±0.01
e
0.73±0.16
fg
0.34±0.00
hi
0.07±0.01
j
ND
0.07±0.00
0.19±0.02 0.55±0.03
gh
c
ND 0.46±0.00
b
ND 0.07±0.01
c
0.44±0.06 0.16±0.01
cd
0.18±0.01
c
0.15±0.03
cd
0.15±0.01
cd
0.09±0.02
efg
0.27±0.01
b
0.30±0.05
b
0.05±0.01
g
ND
0.13±0.00
cde
2.1
2.78
ND 0.34±0.01 ND
ij
17.13
ND
a
ND
b
Tangeretin
Kaemperol
2.00±0.08f
ND
1.55±0.03
gh
0.08±0.00
1.71±0.11
g
0.10±0.00
2.79±0.02
bc
ND
2.92±0.02
b
ND
2.73±0.08
cd
ND
2.49±0.02
e
ND
6.83±0.43a
2.19±0.14f
ND
0.33±0.00hi
4.09±0.14ef
2.55±0.09de
ND
0.12±0.01d
4.20±0.18b
3.85±0.10f
1.45±0.07h
0.08±0.00
0.38±0.01a
1.40±0.00e
4.51±0.26d
2.67±0.30cde
ND
ND 0.06±0.01
f
0.03±0.01
g
ND 0.07±0.02
f
0.10±0.01
e
0.16±0.01
c
0.02±0.00
g
1.52
0.74±0.01
fg
0.13±0.01
ij
0.12±0.00
ij
0.07±0.01
j
0.51±0.03i
0.89±0.02
f
b
20.63
6.23±0.07
b
2.22±0.04
h
2.25±0.03
h
6.49±0.25 66.54
2.02±0.02
f
0.03±0.00
0.87±0.01
i
ND
0.88±0.01
i
ND
0.19±0.01
j
ND
5.56±0.19
a
ND
34.57
0.29
Table 2 The extractable and bound phenolic acid contents in the peels of the 14 wild mandarin genotypes and 2 cultivars analyzed in this study (μg/g DWa)b. Genotypes
PA types c
Benzoic acids Protocatechuic h
p-Hydroxybenzoic
Vanillic
Caffeic
p-Coumaric
173.86±2.69de
28.81±0.52d
642.44±5.28b
7780.17±563.30a
203.14±13.57c
32.58±0.74c
565.22±24.70b
323.73±9.51gh
3711.07±101.08e
180.68±8.37d
25.45±0.76e
76.24±1.76d
460.31±17.92c
212.56±5.03j
2772.10±58.93fg
132.88±1.98gh
19.31±0.90fg
40.16±1.04d
88.28±1.59c
1256.20±80.61a
834.77±29.81a
5438.18±310.18b
ND
21.97±1.32f
18.41±0.55d
21.72±1.58f
57.25±2.50fg
331.57±30.12de
260.54±14.73i
2846.02±203.00f
150.33±12.32fg
8.85±0.19h
WL
12.71±0.55ef
38.10±1.75d
52.70±4.31g
255.36±11.37fg
350.85±10.19g
2447.13±57.97fgh
118.68±4.15h
16.81±1.69g
JJ
12.99±0.53ef
31.50±1.12e
95.09±1.74b
376.53±7.40d
426.05±12.49ef
5022.94±119.41c
157.24±5.22ef
29.19±0.44d
CP
6.26±0.59gh
16.55±3.58g
23.99±4.57i
96.53±15.04h
198.66±30.58j
2155.94±323.15hi
75.80±11.53ij
9.75±0.74h
XP
23.22±0.37c
31.19±1.70e
63.91±4.29e
300.29±5.44efg
487.35±18.81c
4270.57±275.70d
230.11±25.12b
26.75±1.49e
gh
e
g
def
h
DK
3.66±0.50
DX
11.49±0.47ef
49.34±1.42c
60.76±3.78ef
337.24±16.22de
450.97 ±21.23de
ND
19.87±0.38cd
50.64±0.98c
63.67±2.30e
458.53±36.74c
BY No.1
18.30±3.01d
31.42±1.80e
73.28±5.73d
13.26±0.30e
30.46±2.59e
GX
12.62±1.20ef
TG
BY No.2
extractable
84.26±3.16a
117.62±2.86a
249.48±0.57g
464.29±4.41cd
1917.57±32.20ij
152.39±5.63fg
46.68±0.78b
WC
39.02±6.13b
79.72±1.92b
119.28±4.77a
251.71±24.61g
400.25±31.34f
1730.93±156.47j
87.24±14.37i
61.50±4.96a
ST
8.85±1.24fg
29.52±2.66e
45.26±3.49h
46.24±2.89h
154.55±9.79k
1613.34±99.30j
60.79±3.52j
16.79±1.04g
PK
10.68±0.58ef
30.54±0.73e
63.98±0.35e
1273.47±77.61a
416.44±20.96f
3322.97±194.57e
83.13±6.06i
9.29±0.18h
Total
262.17
650.85
1115.64
7083.79
6172.30
56700.01
2236.54
68.58±1.11c
81.44±5.96d
433.40±25.54efg
921.28±34.51fg
6551.71±264.31c
110.07±1.94b
45.18±4.91g
ND
19.57±0.03fg
83.00±5.33b
83.77±6.11d
486.10±20.23ef
1265.87±125.73e
8305.33±675.73b
103.76±7.35bc
37.38±3.44gh
BY No.1
18.63±1.04fg
27.04±2.04def
40.71±2.20h
477.95±4.15ef
586.96±4.31i
4111.24±18.62g
66.97±3.54e
14.51±0.82j
20.98±0.95ef
32.66±2.30def
79.33±3.42de
84.52±7.61d
107.24±12.86de
ND
128.44±4.28c
65.65±5.00
664.77±43.93d
15.68±1.99g
26.15±3.96ef
54.54±7.61fg
462.10±38.06efg
841.94±53.45fg
5249.85±503.07ef
66.32±5.59e
28.31±5.13hi
WL
24.44±2.47cde
35.45±4.71d
66.91±4.92ef
537.03±39.49e
1307.48±101.63de
5578.61±386.36de
54.14±3.51f
19.03±0.05ij
JJ
18.82±0.21fg
33.77±0.93de
78.64±9.38de
358.03±40.29gh
571.93±56.82i
3910.52±256.09gh
55.72±3.81ef
24.72±1.33hij
CP
22.18±1.23def
95.91±7.79a
150.22±11.43b
382.10±3.80fgh
1472.80±43.46cd
8095.63±139.51b
167.23±10.16a
74.20±0.99f
XP
25.98±2.06cd
24.12±1.53f
83.24±6.02d
499.18±54.76e
1724.16±80.22b
7563.51±375.37b
86.30±3.08d
114.21±13.58d
JZ
19.69±2.21fg
63.62±4.84c
103.44±6.98c
1017.21±27.15b
1625.66±76.65bc
6433.09±357.66cd
56.37±2.91ef
25.67±1.51hij
XC
48.06±2.57a
84.36±0.29b
182.81±5.58a
306.14±1.15hi
1278.15±11.85e
4328.05±82.28g
97.59±5.73c
264.93±4.83a
WC
28.29±2.50bc
63.30±3.56c
144.48±8.27b
251.56±15.10ij
853.60±84.23fg
3124.48±236.33h
63.06±5.11ef
175.96±3.84b
ST
31.74±0.26b
78.39±0.04b
43.91±1.76gh
193.19±8.93j
461.33±32.89i
4419.71±278.68fg
34.99±3.81g
ND
PK
21.37±0.55
ef
fg
g
Total
379.74
26.97±2.45 889.78
59.00±5.31 1428.16
908.84±67.08 9505.98
1016.23±71.20 19007.06
f
13607.19±837.02
4548.02±321.60 97871.00
ND, not detectable. a Data are expressed as means ± standard deviation of triplicate samples. b Different superscripts between rows represent significant differences between samples (p < 0.05). c
a
TG
c
3642.63±242.46
6102.41±325.37cde a
24.79±2.32
f
2055.79±137.74
801.45±33.06gh a
GX
def
101.66±9.19
c
100.19±4.06
34.02±4.49gh
19.53±0.94fg
c
5941.67±517.84
381.93 bc
DX
cde
636.61±51.34
cde
19.98±1.64
bound
472.59±51.49
hi
87.43±7.53
DK
BY No.2
74.09±1.51
ef
2363.94±162.75
7.72±0.42h
44.77±3.16a
de
299.94±20.75
i
XC
80.83±1.77
320.24±4.97
gh
6.08±0.32
b
53.75±0.83
3467.14±66.08
e
JZ
f
33.14±2.56
248.92±3.45
i
Sinapic
5839.99 ±259.01b
504.87±5.67
bc
Ferulic
20.51±0.35f
60.57±1.79
ef
Chlorogenic
342.84±1.59a
52.57±0.38
c
Cinnamic acids
PA type are expressed as phenolic acid type
43.52±3.42 1190.74
98.04±0.24e 1191.79
Table 3 The fruit materials, the total phenolic, total flavonoids content (mg/g DWa)b, and antioxidant capacities (μM TE/g DW) of the fruits analyzed in this study. Number
Scientific name
Repository number
Chinese name
Abbreviation
Total phenolics
Total flavonoids
DPPH
FRAP
ABTS
ORAC c
APC indexc
Rank
84.57
3
1
Citrus daoxianensis S.W.He
GPGJ0757
Dakengyeju
DK
45.38±0.82b
9.70±0.29e f
39.95±1.41 b
40.47±2.12 bc
104.22±3.58 a
642.49±34.46
2
Citrus daoxianensis S.W.He
GPGJ0144
Daoxianyeju
DX
43.46±0.35bcd
16.28±0.83b
38.71±3.16 bc
42.90±2.71 ab
91.01±2.87 cd
625.40±20.21 cd
81.69
4
3
Citrus reticulata Blanco
GPGJ0790
Nieduyeju
ND
51.14±0.26a
16.80±0.34b
48.21±1.75 a
46.98±0.89 a
108.60±0.24 a
834.37±16.98 a
98.89
1
4
Citrus reticulata Blanco
GPGJ0785
Banyeshengjuzi No.1
BY No.1
39.86±0.55ef
8.93±0.24fg
36.11±0.11 bcd
34.81±1.50 defg
94.61±5.24 bc
529.42±60.49 efg
74.06
9
5
Citrus reticulata Blanco
GPGJ0782
Banyeshengjuzi No.2
BY No.2
41.43±1.36
de
a
645.30±17.60 c
76.69
6
38.37±1.18
fg
85.00±0.24
def
610.76±8.43
cd
77.83
5
36.02±0.62
gh
88.54±1.91
cd
557.64±7.69
def
29.38±2.63
j
65.62±1.43
g
84.27±1.18
def
91.69±6.67
cd
6 7 8 9 10 11 12 13 14 15 16 a
Citrus reticulata Blanco Citrus reticulata Blanco Citrus reticulata Blanco Citrus reticulata Blanco Citrus reticulata Blanco Citrus reticulata Blanco Citrus reticulata Blanco Citrus reticulata Blanco Citrus reticulata Blanco Citrus unshiu Marc. Citrus poonensis Hort. Ex Tanaka
GPGJ1243 GPGJ0042 GPGJ0402 GPGJ0089 GPGJ0041 GPGJ0036 GPGJ0339 GPGJ0986 GPGJ0030 GPGJ0667 GPGJ00948
Guangxihongpisuanju Tugan Wulongsuanju Jinju Cupigoushigan Xipigoushigan Jizigan Xichuanzhoupigan Wangcangzhoupigan Satsuma Ponkan
GX TG WL JJ CP XP JZ XC WC ST PK
hi
35.27±0.69
12.56±0.31
c
10.34±0.85
e
20.66±1.53
a
8.87±0.32
fg
44.64±2.02
bc
11.55±0.58
42.32±3.28
cd
fg
31.09±1.17
j
13.53±0.94
33.55±1.67
i
8.33±0.26
g
8.12±0.26
g
hi
34.48±0.13 39.71±1.21
ef
36.54±0.63
gh
Data are expressed as means ± standard deviation of triplicate samples. Different superscripts between rows represent significant differences between samples (p < 0.05) c Antioxidant index score = [(sample score/best score) × 100] b
7.95±0.09
g
8.81±0.84
d
c
h
6.28±0.24
10.59±0.12
de
32.05±0.41
de
38.75±0.18
bc
32.59±0.35
de
29.04±1.20
ef
39.45±1.38
bc
50.46±3.57
a
33.59±1.87
cde
33.84±1.64
cde
33.82±0.53
cde
35.15±0.58
bcd
25.14±0.58
f
36.35±1.27
bcd
32.83±0.57
fgh
39.03±0.46
bcd
30.27±0.50
gh
26.50±0.44
h
36.93±1.00
cde
46.55±1.64
a
36.41±2.82
cde
31.15±0.13
gh
30.08±2.96
gh
32.66±2.92
efg
35.06±1.15
defg
35.58±1.05
de
104.27±4.74
101.18±2.62
ab
66.97±2.68
g
77.59±0.72
f
80.45±2.63
ef
87.53±2.11
cde
88.88±3.34
cd
69.34
12
508.85±45.37
efg
58.84
16
421.49±14.29
hi
71.22
11
631.05±43.41
cd
89.78
2
577.72±29.38
cde
76.62
7
395.66±14.42
i
60.61
15
487.85±14.50
fgh
65.49
14
462.03±30.95
ghi
67.16
13
748.21±21.07
b
73.68
10
578.86±27.55
cde
74.74
8
Figure 1
Figure 2
1
China is rich in wild mandarin germplasms which were underutilized.
2
The phenolic and antioxidant activity of main Chinese wild mandarin were reported.
3
Some wild genotypes were rich in phenolics and exhibited high antioxidant capacity.
4
Remarkable variation was observed in phenolics contents and antioxidant capacity.
5
18 individual flavonoids and 8 phenolic acids were identified from studied fruits.