全 文 ：第 50 卷 第 8 期
2 0 1 4 年 8 月
林 业 科 学
SCIENTIA SILVAE SINICAE
Vol. 50，No. 8
Aug．，2 0 1 4
doi:10．11707 / j．1001-7488．20140808
Ｒeceived date: 2013 － 10 － 14; Ｒevised date: 2014 － 06 － 05．
Funded project:The Fundamental Ｒesearch Funds for the Central Universities(XDJK2013C053) ．
* Corresponding author: Xu Li．
新疆药用植物黑桑的抗氧化性*
王传宏 刘 超 刘 静 向 伟 黄先智 徐 立
(西南大学生物技术学院 重庆 400715)
摘 要: 为寻找一种天然的抗氧化材料，以新疆药用植物黑桑的根、枝、叶和果实的乙醇提取物为材料，进行总多
酚、总黄酮、抗氧化能力以及螯合 Fe2 + 测定。结果显示: 果实(桑椹)提取物(EEMF)的总多酚含量(0. 943 8 mg·
mL － 1 )以及总黄酮含量(0. 174 7 mg·mL － 1 )与叶提取物(EEML)、枝提取物(EEMB)和根提取物(EEMＲ)相比并不
高，但 EEMF 的抗氧化能力最强，其清除羟基自由基、DPPH 自由基能力分别达到 96. 46%，96. 83%，抑制脂质体氧
化能力达到 71. 14% ; 此外，EEMF 螯合 Fe2 +能力也强于其他 3 种。表明黑桑 4 个部位都具有良好的抗氧化能力，
且果实最佳。
关键词: 药桑; 黑桑; 总多酚; 总黄酮; 抗氧化性; 螯合 Fe2 +
中图分类号: S718. 43 文献标识码: A 文章编号: 1001 － 7488(2014)08 － 0053 － 07
Antioxidant Activity of Medicine Mulberry (Morus nigra) in Xinjiang
Wang Chuanhong Liu Chao Liu Jing Xiang Wei Huang Xianzhi Xu Li
(College of Biotechnology，Southwest University Chongqing 400715)
Abstract: In order to find a natural antioxidant material，ethanolic extracts of fruits ( EEMF)，leaves ( EEML)，
branches (EEMB) and roots (EEMＲ) of medicine mulberry(Morus nigra) were investigated． The results showed that
although the medicine mulberry fruits did not have the highest total polyphenol content (0. 943 8 mg·mL － 1 ) and total
flavonoids content (0. 174 7 mg·mL － 1 ) among those organs，the EEMF possessed the strongest antioxidant effect． The
abilities of scavenging hydroxyl radicals，scavenging DPPH radicals and inhibiting lipid oxidation reached to 96. 46%，
96. 83% and 71. 14%，respectively． In addition，Fe2 + chelating ability of EEMF was stronger than that of EEMＲ，EEMB
and EEML． Therefore，medicine mulberry fruit can be used to develop a natural and nutritious food additive．
Key words: medicine mulberry; Morus nigra; total polyphenols; total flavonoids; antioxidant activity; Fe2 + -chelating
activity
Ｒeactive oxygen species ( ＲOS )，kinds of active
chemical materials which were generated by the biological
oxidation，includes O2
－，H2O2，·OH and so on ( Sies，
1986) ． With the process of oxidation in vivo，ＲOS will
result in the damage to all kinds of biological
macromolecules，such as protein，fat，and DNA (David et
al．，1997; Shukla et al．， 2009 ) ． Furthermore， this
damage is also likely to contribute to the decline and death
of cells， coronary heart diseases， atheromas， cancers，
diabetes，arthritis，neurological disorders etc ( Germanas
et al．，2007; Devasagayam et al．，2004; Finkel et al．，
2000) ．
Many synthetic antioxidants such as butylated
hydroxyanisole ( BHA ) and butylated hydroxytoluene
( BHT )，which have been proved to possess potential
health risk to human beings ( Botterweck et al．，2000 )，
are hoped to be replaced by some natural antioxidants．
Ｒecent studies suggest that blueberry and apple extracts
could prolong the life of fruit flies ( Peng et al．，2012;
2011)，and daily consumption of blueberry juice would
improve elderly people’s memory function ( Krikorian et
al．，2010 ) ． All of these functions result from the great
antioxidant capacity of natural products． Furthermore，
plants’ substances with great antioxidant capacities and
health benefits have been extracted from persimmon skin，
orange peel，tea，grape seeds and skins，even some of
林 业 科 学 50 卷
which are of great interest in the industry after they are put
into practice (Wolfe et al．，2003; Bocco et al．，1998;
Tang et al．，2002; Yusuf et al．，2004) ．
Medicine mulberry ( Morus nigra ) which is rarely
seen in nature is the only black mulberry in China．
Medicine mulberry is regarded as folk medicine by Uygur
people，ethanol extracts of whose fruits have been drinking
to keep fit for a long time，and its fruits are often used as
anti-pharyngitis drugs． However， reports on the
antioxidant activity of extracts from each part of it are still
unknown． Therefore，this investigation is going to explore
the antioxidant activity of the extracts of Medicine
mulberry’s fruits，branches，leaves，and roots，in terms
of total polyphenols content，total flavonoids content，free
radical scavenging capacity and Fe2 + -chelating activity，
aiming to find a new natural green food antioxidant and lay
a foundation for the future reasonable development of
Medicine mulberry．
1 Materials and methods
1. 1 Materials
Ascorbic acid ( Vc )， gallic acid， rutin， 1，1-
diphenyl-2-picrylhydrazyl ( DPPH ) and lecithin were
purchased from Sigma (St． Louis，Mo，USA); potassium
ferricyanide， ferrozine， thiobarbituric acid ( TBA )，
phosphoric acid， ethanol， sodium hydroxide，
trichloroacetic acid ( TDA )， sodium carbonate were
purchased from Kelong ( Chengdu， Sichuan， China );
iMark microplate reader ( Japan )，FA2004A electronic
balance ( Shanghai，China)，B． U Chi Ｒ-210 rotavapor
(Flawil，Switzerland) ．
The samples of Medicine mulberry ( Morus nigra )
were collected from Xinjiang Hetian Sericulture Science
Institute in November 2012． The leaves，branches and
roots were dried at 50 ℃ and the fruits stored in － 80 ℃
refrigerator．
1. 2 Sample preparation
Each sample ( 20 g ) was powdered at low
temperature and extracted with 200 mL 75% ( V /V )
ethanol，for 2 h，3 times，and the filtrate was evaporated
to dryness until the weight would never change． The dried
extracts of each sample were named as EEML，EEMB，
EEMF and EEMＲ ( ethanolic extracts of mulberry leaves，
branches，fruits and roots，respectively) ． The volume was
adjusted with 75% (V /V) ethanol to 500 mL． Percentage
yields of EEML，EEMB，EEMF and EEMＲ of dry weight
were 20. 16%，7. 7%，86. 76% and 17. 65% ( w /w)，
respectively．
1. 3 Total polyphenols content
Total polyphenols content was estimated by using the
Folin-Ciocalteu colorimetric method described previously
but with a slight modification (Bae et al．，2007) ． 0. 1 mL
extract was mixed with 0. 1 mL Folin-Ciocalteu reagent
( 50%， V /V )， shaken vigorously， and after 5 min
reaction，3 mL Na2 CO3 ( 0. 2 g·mL
－ 1 ) was added into
each mixture． The reaction mixture was incubated at 20 ℃
for 2 h． The absorbance was determined at 765 nm．
Ｒesults were compared with a gallic acid calibration curve
and expressed as milligram of gallic acid equivalent per
one mL of extracts．
1. 4 Total flavonoids content
The total flavonoids content assay was carried out by
the previously described way with a few modifications and
used rutin as a standard flavonoid (Hairi et al．，1991) ．
0. 5 mL (50 mg·mL － 1 ) NaNO2 was added into 0. 1 mL
extract and shaken vigorously，leaving the mixture at room
temperature for 6 min，and then，0. 5 mL Al(NO3 ) 3 was
added into reaction mixture． After 6 min standing，2. 5
mL NaOH was mixed together with mixture and left at
room temperature for 15 min． The absorbance was
determined at 510 nm． Ｒesults were compared with a rutin
calibration curve and expressed as milligram of rutin
equivalent per one mL of extracts．
1. 5 Ｒeducing activity
The reducing power assay was in accordance with the
previous reference ( Yen et al．，1995 ) ． 80 μL extracts
were added to 1 mL phosphate buffer ( pH6. 6 )，1 mL
potassium ferricyanide (10 mg·mL － 1 ) was mixed with the
buffer and incubated at 50 ℃ for 20 min before having a
ice-water bath． Soon afterwards，1 mL trichloroacetic acid
(100 mg·mL － 1 ) and 1 mL ferric chloride (1 mg·mL － 1 )
were added to the mixture in turn，shaken vigorously． The
absorbance was determined at 700 nm after 10 min
incubation and compared with an ascorbic acid calibration
curve．
1. 6 DPPH radical scavenging capacity
The assay was carried out following the previously
described approach with a few modifications ( Chu et al．，
2000) ． Different volumes of extracts (20，50，80，100，
200，300，400 μL ) were reacted with 250 μL DPPH
respectively，and then the total volume was adjusted with
70% (V /V) ethanol to 4 mL and shaken vigorously． After
45
第 8 期 王传宏等: 新疆药用植物黑桑的抗氧化性
incubated at 25 ℃ for 10 min， the absorbance was
determined with a Microplate reader at 517 nm． A lower
level of absorbance indicated a stronger scavenging
activity． The scavenging ability was calculated according
to following formula: Scavenging effect (% ) =［1 － ( A s /
A c)］ × 100． Where A c is the absorbance of the control
groups and A s is the absorbance in the presence of
extracts．
1. 7 Hydroxyl radical scavenging
According to the previous reference with a few
modifications ( Jeong et al．，2009)，1. 5 mL FeSO4 (1. 5
mmol·L － 1 ) and 1 mL H2O2 (6 mmol·L
－ 1 ) were mixed
together， then water bath in 37 ℃ ． After 30 min，
hydroxyl radical was generated from Fenton reaction． 0. 5
mL salicylic acid ( 20 mmol·L － 1 ) as well as various
volume extracts were added into the mixture and the total
volume was adjusted with 70% ( V /V) ethanol to 4 mL，
allowed to react for 1 h at 37 ℃ ． The absorbance was
determined at 562 nm． A lower level of absorbance
indicated a stronger scavenging ability．
The percentage of hydroxyl radical was calculated by
using the formula given below: Scavenging effect (% ) =
［1 － (A s /A c)］ × 100． Where A c is the absorbance of the
control and A s is the absorbance in the presence of extracts
or other scavenger．
1. 8 Fe2 + -chelating activity
According to a literature procedure， the assay was
measured but with a few modifications ( Chang et al．，
2011) ． Fe2 + -chelating ability of extracts was monitored by
the absorbance of the ferrous iron-ferrozine complex at 562
nm． Different volumes of extracts (100 － 700 μL) were
added into 1 mL FeCl2 (0. 2 mmol·L
－ 1 ) ． The reaction
was initiated by the addition of 0. 5 mmol·L － 1 ferrozine
(0. 1 mL) dissolved in filled water，then the total volume
was adjusted with 70% ( V /V ) ethanol to 4 mL． The
absorbance of the Fe2 + -ferrozine complex was measured at
562 nm against a blank group． A lower level of absorbance
indicated a stronger chelating activity．
1. 9 Inhibiting lipid oxidation activity
According to the reference described previously with
a few modifications (Tamura et al．，1991)，lecithin (300
mg) was dissolved in 30 mL phosphate buffer (10 mmol·
L － 1，pH7. 4) by using an ultrasonic cleaner，which was
carried out in ice-water． Different volumes of extracts
(0. 2 － 1. 2 mL) were mixed with 1 mL sonicated solution
(10 mg·mL － 1 )，1 mL FeCl3 (0. 4 mmol·L
－ 1 ) and 1 mL
ascorbic acid (0. 4 mmol·L － 1 )，then the total volume was
adjusted with 70% (V /V) ethanol to 4. 5 mL and shaken
vigorously． The mixture was added into 2 mL TCA-TBA-
HCl after incubated at 37 ℃ for 60 min in a dark place，
the centrifuge tubes were put into boiling water for 15
min，which was then in ice-cold water bath for 5 min and
centrifuged at 5 000 r·min － 1 for 5 min． The absorbance of
supernatant was measured at 532 nm． The blank group
contained all reagents except lecithin． A lower level of
absorbance indicated a stronger protective activity．
Inhibiting lipid oxidation capacity of each sample was
calculated via the formula: Inhibition (% ) =［1 － ( A s /
A c)］ × 100． Where A c is the absorbance of the control
and A s is the absorbance in the presence of extracts．
1. 10 Statistical analysis
Each experiment was carried out in triplicate． The
data were analyzed by SPSS ( version 18. 0) and expressed
as means  tandard deviation ( SD ) ． Ｒesults were
considered significantly at P ＜ 0. 05．
2 Ｒesults and discussion
2. 1 Total polyphenols content and total
flavonoids content
According to the regression equations of gallic y =
1. 212 3x + 0. 033 5 (Ｒ2 = 0. 999 9)，the concentration
of the total polyphenols was calculated． As is shown in
Fig． 1， EEMＲ has the highest concentration of
polyphenols， reaching1. 643 4 mg·mL － 1， and EEML
contains the lowest polyphenols，only 0. 247 9 mg·mL － 1 ．
In other words，each gram of dry extract contains 30. 74
mg ( EEML )， 222. 32 mg ( EEMB )， 232. 84 mg
( EEMＲ ) and 27. 20 mg ( EEMF ) of polyphenols
separately．
Fig． 1 Total polyphenols content and total flavonoids
content of each sample
55
林 业 科 学 50 卷
On the basis of the regression equations of rutin y =
0. 419 5x － 0. 009 3 (Ｒ2 = 0. 999 7)，the concentration of
the flavonoids content were calculated． Just as the content
of total polyphenols，EEMＲ also has highest content of
flavonoids． Fig． 1 shows EEMＲ contains the highest total
flavonoids content，reaching 0. 801 7 mg·mL － 1 ． The total
flavonoids content in these extracts are in the order of
EEMＲ ＞ EEMB ＞ EEMF ＞ EEML． The high content of
polyphenols and flavonoids is far more than those in other
tested mulberry (Chang et al．，2011) ． It has been widely
recognized that due to the free radical scavenging capacity
and strong reducing power of polyphenols in vivo (Birt et
al．，2001)，it has the function of inhibiting atherosclerosis
and tumor cell proliferation ( Cheung et al．， 2003 ) ．
Therefore，the main reason why the mulberry branches and
roots have been regarded as an herbal medicine is the
abundant polyphenols in them． Besides，the difference of
polyphenols content and flavonoids content indicated that
the four samples of polyphenols not only exist as
flavonoids．
2. 2 Ｒeducing power
There are linear regressions and a significant
relationship between total flavonoids and reducing power in
all extracts． It can be obviously found in Tab． 1 that
EEMF has strongest reducing power，which was about
1. 17-fold，2. 82-fold， 7. 37-fold， greater than that of
EEMＲ，EEMB and EEML respectively． Except EEMF，
the polyphenols and flavonoids content of EEMＲ，EEMB
and EEML were significantly correlated with reducing
power， the linear correlation coefficient of total
polyphenols and reducing power is r = 0. 998 0，and the
total flavonoids content correlated extraordinarily well
(Fig． 2 ) ． Furthermore， as is shown in Tab． 2， the
reducing power of different concentration of EEMF，
EEMＲ，EEMB and EEML were noticeably correlated with
total flavonoids． In many vitro studies，polyphenols and
flavonoids compounds were demonstrated the main material
of antioxidant activities (Chew et al．，2009; Socha et al．，
2009; Proestos et al．，2006) ． Our data are consistent with
the previous studies．
Tab． 1 IC50 in DPPH radical，·OH radical (mg·mL
－ 1 )，
maximum inhibition rate of lipid oxidation (%) and reducing ability①
Samples DPPH ·OH radical Lipid Ｒeducing ability*
EEMF 0. 108 ± 0. 009 c 0. 561 ± 0. 016 c 71. 138 ± 2. 333 a 2. 144 ± 0. 115 a
EEMＲ 0. 140 ± 0. 016 c 1. 841 ± 0. 077 b 37. 777 ± 4. 126 b 1. 839 ± 0. 020 b
EEMB 0. 337 ± 0. 017 b 3. 004 ± 0. 136 a 33. 746 ± 5. 328 bc 0. 759 ± 0. 036 c
EEML 1. 400 ± 0. 050 a 1. 760 ± 0. 104 b 30. 975 ± 2. 199 c 0. 291 ± 0. 018 d
Vc 0. 017 ± 0. 003 d 0. 026 ± 0. 044 d — —
①Column wise values with same letter indicate no significant difference (P ＞ 0. 05) ． Ｒesults are displayed with means  tandard deviations for n =
3． * Expressed as ascorbic acid equivalent．
Tab． 2 The linear regressions of different concentration
flavonoids and reducing power
Samples Linear regressions
EEML Y = 0. 002 7 x + 0. 021 0(Ｒ2 = 0. 998 9)
EEMB Y = 0. 005 9 x + 0. 042 0(Ｒ2 = 0. 999 2)
EEMＲ Y = 0. 012 2 x + 0. 139 1(Ｒ2 = 0. 998 8)
EEMF Y = 0. 017 1 x + 0. 055 8(Ｒ2 = 0. 998 9)
2. 3 DPPH radical，hydroxyl radical scavenging capacity
The capability of scavenging radical is regarded as
one of the regular indexes of evaluating the ability of
antioxidant activity． Among the ＲOS，hydroxyl radical is
the most reactive and induces severe damage to bio-
molecules ( Sakanaka et al．， 2005 ) ． Because of the
hydroxyl radical’s high reactivity which enables itself to
react with a wide range of molecules found in living cells
such as amino acids， sugars， lipids and nucleotides，
hydroxyl radical scavenging is an important antioxidant
Fig． 2 Linear regressions of reducing power and
flavonoids concentration
activity (Stohs et al．，1995) ． From the Fig． 3，it can be
easily found EEMF has the strongest capacity of
scavenging·OH radical，which may as a result of the high
content of anthocyanins， which had the functions of
excellently resisting oxidation， getting rid of hydroxyl
65
第 8 期 王传宏等: 新疆药用植物黑桑的抗氧化性
radicals(Kang et al．，2006) ．
Fig． 3 Scavenging hydroxyl radical activity of the samples
Besides， the four extracts have similar ability of
scavenging radical． As is shown in Fig． 4，four extracts all
possess the ability of scavenging DPPH radical． Although
EEMＲ，EEMB and EEML have the similar trend in the
reaction system， EEMF has the strongest scavenging
capacity obviously， it can be demonstrated IC50 in the
Tab． 1．
Fig． 4 Scavenging DPPH effects of the samples
2. 4 Inhibition lipid oxidation capacity
Fig． 5 implies that the abilities of inhabiting lipid
oxidation of the four extracts are remarkably different．
With the increasing concentration， the capacities of
inhabiting lipid oxidation were on the increasing trend，
and EEMＲ and EEMF were stronger than EEML and
EEMB at the same concentration． Moreover， anti-lipid
oxidation capacity of EEMF was proportional to the
concentration， and EEMＲ exhibited the strongest
capability by 37. 78%， while EEMF was 71. 14%，
revealing that EEMF is the most effective in preventing
lipid oxidation in vitro． Lipid oxidation is a harmful
process occurring in a cell’s physiological metabolism．
Induced by ＲOS， lipid oxidation will lead to cellular
damage and promote the pathological progression of
carcinogenesis，atherosclerosis and diabetes (Wang et al．，
2007) ． Medicine mulberry fruit wine is seen as high-end
nutritional nourishment by Uygur． In the experiment，
EEMF’s ability to inhibit the oxidation of lipid is stronger
than that of the others，which will contribute to the cell
membrane antioxidant， aging prevention and
pigmentation．
Fig． 5 Liposome protection of the samples
2. 5 Fe2 + -chelating activity
Compared with the control group，it was easily found
all of the extracts have Fe2 + -chelating activity from Fig． 6．
Obviously，EEMＲ and EEMB have chelating activities，
meanwhile EEMF and EEML even have stronger chelating
activities than theirs． Although as the essential metal
element for the body，iron contains an unpaired electron，
so that they are able to participate in the single-electron
transfer reactions，which is harmful to human body (Lloyd
et al．，1997) ． It can be figured out from this experiment
that despite the same chelating Fe2 + function of the four
extracts，chelating ability of EEMF is much stronger． So
EEMF can replace deferoxamine which is the only iron
chelator in clinical used for the treatment of iron overload
disease．
Although the content of total flavonoids in EEMF is
lower than that in EEMＲ，EEMB and EEML，EEMF’s
reducing power is more powerful than that of others．
According to some reports，per 100 grams of fruits extract
liquid have the content of 418 mg of VC and 6. 2 g of
reducing sugar (Maimaiti et al．，2007) ． Apart from that，
it was found that Medicine mulberry fruits possess higher
content of antioxidants，such as β-carotene，VB and VE
(Maimaiti et al．，2002 ) ． Besides，anthocyanins content
in Medicine mulberry fruits reached 0. 02% ( w /w )
( Jiang， 2010 ) ． The main antioxidant physiological
75
林 业 科 学 50 卷
Fig． 6 Fe2 + -chelating activity of the samples
function of anthocyanins is scavenging free radicals，
studies have shown that the antioxidant capacity of
anthocyanins is 20 times higher than the VE，50 times
higher than VC， and even stronger than that of rutin
( Jiang，2010; Tsuda et al．，2003; Wang et al．，2000) ．
Whats more， anthocyanins could protect cells from
damage，and prevent lung cancer cell proliferation (Chen
et al．，2006) ．
A large number of Medicine mulberry(Morus nigra)
are planted in Xinjiang to fix sands． However，because of
the heavy drug smell of their leaves，the leaves can not be
used to feed silkworms． A great quantity of branches were
cut down every year，but they only to use as firewood，this
is not only a waste lots of resources，but also produces
environmental pollution． From this investigation，
Medicine mulberry could be developed into a kind of
antioxidant additives which are new and green．
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