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Industrial Crops and Products 83 (2016) 255267

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Industrial Crops and Products


journal homepage: www.elsevier.com/locate/indcrop

Phytochemical content and antioxidant activity of different fruit parts


juices of three gs (Ficus carica L.) varieties grown in Tunisia
Arij Harzallah , Amira Mnari Bhouri, Zahra Amri, Hala Soltana, Mohamed Hammami
Biochemistry Laboratory, Research Laboratory LR12ES05: Lab-NAFS NutritionFunctional Food & Vascular Health, Faculty of MedicineUniversity of
Monastir, Tunisia

a r t i c l e i n f o a b s t r a c t

Article history: Fig is an important source of bioactive compounds and has been a typical component in the health-
Received 2 October 2015 promoting Mediterranean diet for many centuries.
Received in revised form This study was conducted to evaluate differences between phytochemical composition and antioxidant
15 December 2015
properties of juices of peel, pulp and total fruit of gs from three different varieties grown in Tunisia
Accepted 16 December 2015
Mediterranean coast and corresponding to three different colors (green, purple and black) as well as the
Available online 22 January 2016
effect of maturation stage on the amounts of phytochemical composition including total phenols content
(TPC), total avonoids content (TFC), total ortho-diphenols content (TOPC), total tannins content total
Keywords:
Ficus carica L.
(TTC) and total anthocyanins content (TAC).
Fig juice Antioxidant potential was assessed by two assays: 1,1-diphenyl-2-picrylhydrazyl (DPPH) scaveng-
Phytochemical content ing capacity and reducing power (RP) and showed that different g juices extracts exhibited the same
Antioxidant activity antioxidant capacity in both systems tested and at different concentrations.
Fruit color Black peel juice acted as the greatest antioxidant by having the highest DPPH and RP activities followed
by the juice of black g total fruit. The antioxidant capacities observed were attributed to higher total
phenolic, avonoid and anthocyanin contents according to the chemometric results.
Comparison of phytochemical composition of g fruits during the development stage revealed a sig-
nicant increase of TPC, TFC, TOPC, TTC and TAC in the ripe fruits of the three tested varieties.
This is the rst study comparing the phytochemical composition and antioxidant potential of juices of
Ficus carica L. peels, pulps and total fruits.
2015 Elsevier B.V. All rights reserved.

1. Introduction Figs were analysed for total polyphenols, total avonoids and
exhibited high anti-oxidant capacity (Solomon et al., 2006). It is a
The g tree (Ficus carica L.) was evidently originated in the Mid- very nourishing food and used in industrial products. It is rich in
dle East (Mars, 2001). Most of the worlds g production occurs in vitamins, mineral elements, water, and fats. It is one of the highest
the Mediterranean countries (Sadder and Ateyyeh, 2006), where plant sources of calcium and ber (Joseph and Raj, 2011). They are
diets are characterized by abundant intake of g fruit (Solomon rich in easily digestible natural sugars, and contain rich amounts
et al., 2006). Tunisia is one of the most important consumers of of anthocyanins and avonoids that contribute to gs coloration
gs. F. carica L. is present all over Tunisia in various environmental (Solomon et al., 2006) and to signaling pathways regulation that
conditions. The tree grows well and produces tasteful and avour- guide cellular metabolism. Humans have eaten the fruits of this tree
ing fruits enhanced by warm and shiny conditions during ripening from the earliest times, and utilized it and its by-products (leaves,
(Trad et al., 2012). latex, bark, and roots) in various disorders such as gastrointestinal
respiratory, inammatory, cardiovascular disorders, ulcerative dis-
eases, cancers (Canal et al., 2000; Joseph and Raj, 2011), as laxative,
antispasmodic remedies (Guarrera, 2005), antiviral, an tibacterial,
hypoglycaemic, and anthelmintic effects (Jeong et al., 2005; Joseph
Abbreviations: TPC, total polyphenols content; TFC, total avonoids content;
TTC, total tannins content; TOPC, total O-diphenols content; TAC, total anthocyanins and Raj, 2011).
content; (DPPH) scavenging capacity, 1,1-diphenyl-2-picrylhydrazyl scavenging In another hand, gs can be eaten dried, fresh, as a jam or also as a
capacity assay; RP, reducing power assay; PCA, principal component analysis. juice. Figs are often peeled; the pulp is eaten and the peel discarded
Corresponding author.
E-mail address: harzallaharij@yahoo.fr (A. Harzallah).

http://dx.doi.org/10.1016/j.indcrop.2015.12.043
0926-6690/ 2015 Elsevier B.V. All rights reserved.
256 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 1. Color appearance of the three g varieties examined in this study.

(Veberic et al., 2008), however, in different countries like Tunisia, For every variety, three repetitions were carried out (n = 3); each
consumers prefer to eat the whole fresh fruit. repetition included 10 fruits sampled from three trees.
Most of the previous scientic studies have been focused mainly An agricultural technician performed identication of fruit vari-
on dried gs (Vinson et al., 2005; Vallejo et al., 2012), on fresh gs eties. Fruits were placed in a 4 C refrigerated box and transported
to determine their total phenolic prole and antioxidant capacity within 3 h to the Herbarium of the Laboratory of Biochemistry, Fac-
(Veberic et al., 2008; Vallejo et al., 2012), and also on g leafs to ulty of Medicine of Monastir, Tunisia. There, fruits were washed
describe their antimicrobial activity (Jeong et al., 2009; Lee and with water, wiped completely dry and stored at 20 C until prepar-
Cha, 2010; Ahmad, 2013) or anti-HSV effect (Joseph and Raj, 2011), ing samples the next day.
neglecting the other edible parts. However, there is few data com-
paring the phytochemical content changes occurring in the g fruit
during ripening (Veberic et al., 2008; Crisosto et al., 2010), as well 2.2. Sample preparation
as, in spite of the few researches describing the distribution of
the phenols content between gs pulp and peel (Solomon et al., To prepare whole g juice, 10 ripe gs (2nd crop) from each
2006; Del Caro and Piga, 2008), no data described neither the whole variety were mixed. An equal portion of ripe gs from each variety
phytochemical composition in the g fruit including total phenols was peeled manually with a knife, paying attention not to include
content (TPC), total avonoids content (TFC), total ortho-diphenols the fruit pulp. Peel and pulp were mixed separately too. A blender
content (TOPC), total tannins content total (TTC) and total antho- (Moulinex, France) was used to obtain peel juice, pulp juice and
cyanins content (TAC), nor the antioxidant potential of juices of whole fruit juice. In the blender, the three compartments were
different g fruit parts. juiced. The juice was centrifuged at 3.000 rpm for 10 min; the super-
Thus, to improve the knowledge on g compositions and to val- natant was kept and ltered through a lter. The ltered juices were
orise it as a functional food, the aim of this study is rstly to evaluate stored at 20 C until preparing methanolic extracts the following
the entire phytochemical composition as well as the antioxidant day. Different g juices samples are shown in Fig. 2.
capacities of juices of different ripe g fruit parts including peel, To evaluate the effect of ripening stage on the phytochemical
pulp and total fruit of the most abundant varieties in Tunisia cor- content of gs, 10 ripe and 10 partially ripe gs from each variety
responding to three different colors: black, purple and green; and were homogenized and used.
secondly, to evaluate the inuence of the variety and the crop tim-
ing on the phytochemical composition level of fresh ripe g fruit.

2. Materials and methods

2.1. Plant material

Fresh g fruits (F. carica L.) were manually picked from a same
farm in Bekalta, (coastal town, governorate of MonastirCentral
East part of Tunisia) in 2 different ripening stages: partially ripe
at the beginning of July 2013 (1st crop) and at ripening time at
the last of August 2013 (2nd crop). Specimens were chosen from
three varieties corresponding to three different colors as following
(Figs. 1 and 2):

Kohli variety is a dark type, black in color with dark red pulp. Fruit
are sweet and juicy.
Hamri variety is a dark type, purple in color with light red pulp.
Fruit are sweet and juicy. Fig. 2. Appearance of different fruit parts juices of the three g varieties examined
in this study.
Bidhi variety is a light type, green in color with dark red pulp.
A1: Bidhi pulp, A2: Bidhi total fruit, A3: Bidhi peel, B1: Hamri pulp, B2: Hamri total
Fruit are sweet and juicy. fruit, B3: Hamri peel, C1: Kohli pulp, C2: Kohli total fruit, C3: Kohli peel.
A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267 257

Fig. 3. Bar graphics comparing total polyphenols content (TPC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars
with different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

Fig. 4. Bar graphics comparing total avonoids content (TFC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars with
different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

2.3. Methanolic extracts preparation 2005; Lenucci et al., 2006; Bakar et al., 2009). Extract (1 ml) was
mixed with 4 ml of distilled water in a test tube followed by addi-
Each sample (5 g) was homogenized in 5 ml of methanol until tion of 0.3 ml of 5% sodium nitrate solution and allowed to react for
uniform consistency, using an Ultra-Turrax homogenizer (IKA, T25, 5 min. Then 0.3 ml of 10% aluminum chloride solution was added.
digital). The homogenates were centrifuged at 3000 rpm for 13 min. After 6 min, 2 ml of 1 M sodium hydroxide was added. The mix-
The supernatants were recovered, ltered using 0.45 m lter and ture was diluted with distilled water up to 10 ml and then mixed
stored at 20 C until further analysis within a maximum period of well using a vortex. The absorbance was immediately recorded at
one week. 510 nm.
The absorbance was measured immediately at 510 nm using a
2.4. Determination of total phenols content (TPC) spectrophotometer and the avonoid content was expressed as mg
of Catechin equivalents per gram of fresh weight (mg CE/g FW). All
The method of Montedoro et al. (1992) with slight modications the tests were carried out in triplicate.
was used to determine total phenolic content. Each extract (0.1 ml)
was combined with water 1:4 (v/v) and 2.5 ml FolinCiocalteus 2.6. Determination of total O-diphenols content (TOPC)
phenol reagent (1/10) and incubated for one minute at room tem-
perature, followed by the addition of 2 ml of sodium carbonate Total ortho-diphenol content was determined using the method
(7.5%). The mixture was well shaking and standing for 6 h. The described by Bahorun et al. (1996). Test sample (100 l) was mixed
absorbance of the solutions was measured at 765 nm using a spec- with 1 ml of HCl (0.5N), 1 ml of (NaNo2 + Na2 MoO4 2H2 O) solution
trophotometer (Lambda 25, UV/vis Spectrometer). Values of TPC and 1 ml of NaOH (1 M). The mixture was stirred and kept for half
were estimated by comparing the absorbance of each sample with an hour at room temperature in the dark. The absorbance was
a standard response curve employing six different Gallic acid stan- measured at 500 nm against the blank. Different concentrations
dard solutions, in the same conditions reported for the methanolic of hydroxytyrosol solution were used for calibration. Results were
extract. Results are expressed as milli gram gallic acid equivalents expressed as milli gram of hydroxytyrosol equivalents per gram of
per gram of fresh weight (mg GAE/g FW). Samples of each extraction fresh weight (mg hydroxytyrosol/g FW).
were analysed in triplicate.
2.7. Determination of total tannins content (TTC)
2.5. Determination of total avonoids content (TFC)
Total tannins content were determined spectrophotometrically
Total avonoid content was quantied using the colorimetric according to Broadhurst and Jones (1978). A 0.5 ml of aqueous
method with aluminum chloride according to (Marinova et al., extract, contained in a test tube covered with aluminum foil, was
258 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 5. Bar graphics comparing total ortho-diphenols content (TOC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars
with different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

Fig. 6. Bar graphics comparing total tannins content (TTC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars with
different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

mixed with 3 ml of 4% vanillinmethanol solution and then with 2.9. DPPH free radical scavenging activity
1.5 ml of hydrochloric acid. The mixture was allowed to stand for
15 min at 20 C in the dark. The absorbance of the mixture was The hydrogen atom or electron-donation ability of the F. car-
measured at 500 nm. ica extracts was determined using 1,1-diphenyl-2-picrylhydrazyl
A different concentration of tannic acid aqueous solution (DPPH) free radical as a reagent according to the method of Braca
(30 mg/l) was used for calibration. The nal results were expressed et al. (2001) with minor modication. Briey, 3 ml of solution of
as milli gram tannic acid equivalents per gram of fresh weight (mg DPPH radical in methanol was mixed with 1 ml of g juice extract
TAE/g FW). at different concentrations (220 mg/ml).
The mixture was shaken vigorously and incubated for 30 min in
the dark at room temperature before measuring the absorbance.
The scavenging capacity was determined spectrophotometri-
2.8. Determination of total anthocyanins content (TAC)
cally by monitoring the decrease in absorbance at 517 nm against
a blank using a spectrophotometer (Bio-Rad SmartSpec Plus). The
Total anthocyanin content was quantied according to
percent DPPH scavenging effect was calculated using the following
Padmavati et al. (1997) and Chung et al. (2005).
equation:
Anthocyanins were extracted from 0.5 g of fresh weight with
20 ml methanol/water: concentrated HCl (80/20/1). Samples were Acontrol Asample
put on a shaker in the dark at room temperature for 24 h; DPPH scavenging effect(%) = 100
Acontrol
absorbance (A) was measured spectrophotometrically with the fol-
lowing equation: where Acontrol is the absorbance of the control reaction containing
A = A530 (0.24 A657) , (Gould et al., 2000) where A530 is all reagents except the tested compound. Asample is the absorbance
the absorbance at 530 nm and A657 is the absorbance at 657 nm. of the test compound.
Total anthocyanin content was calculated as mg Cyanidin-3- The results were reported as EC50 value, the effective concen-
glucoside equivalents per 100 g of fresh weight by the following tration of antioxidant agent (extract) providing inhibition 50% of
equation: the initial DPPH radical concentration. EC50 was calculated from
TAC = AMWVDF100
100
, (Giusti and Wrolstad, 2001) where the graph-plotting inhibition percentage against extract concentra-
A = absorbance, MW = molecular weight (449.2 g/mol), tion. The lowest EC50 value indicates the strongest ability of sample
DF = dilution factor, and = molar absorbance coefcient to act as an antioxidant. Ascorbic acid was used as an antioxidant
(26,900 L/mol/cm). All measurements were done in triplicate. standard. Tests were carried out in triplicate.
A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267 259

2.10. Reducing power assay who reported that total phenolic content of Kadota pulp (green
variety) was signicantly higher compared with peel. Among vari-
The reducing power of methanolic extracts of g juices was eties, dark fruits (black and purple gs) showed higher polyphenols
determined by the method of Oyaizu (1986). Substances, which content than the light ones (green g). Differences observed were
have reduction potential, react with potassium ferricyanide (Fe3+) statistically signicant (p < 0.05).
to form potassium ferrocyanide (Fe2+), which then reacts with fer- Flavonoids are important for human health because of their
ric chloride to form ferric ferrous complex that has an absorption high pharmacological activities as radical scavengers (Bakar et al.,
maximum at 700 nm according to the following equation: 2009). The total avonoid content (TFC) is mentioned in Fig. 4 are
Antioxidant
expressed in terms of (mg CE/g FW). Peel of Kohli variety showed
Potassium ferricyanidine + Ferric chloridePotassium the highest concentration of avonoids (12.75 mg CE/g FW). Mean-
while, in Hamri variety avonoids were concentrated in total fruits
ferrocyanide + Ferrous chloride
(11.30 mg CE/g FW). However, in Bidhi variety, avonoids exhib-
ited the lowest concentration compared to the other varieties with
Different concentrations (220 mg/ml) of g juice extract similar amounts in different juices parts.
(2.5 ml) were mixed with sodium phosphate buffer (2.5 ml, 0.2 M, Statistically signicant differences in ortho-diphenol content
pH 6.6) and potassium ferricyanide [K3 Fe (CN)6] (2.5 ml, 1%). The (TOPC) were found between dark and light varieties (p < 0.05)
mixture was incubated at 50 C for 20 min. After cooling, 2.5 ml of (Fig. 5). TOPC in the peels ranged from 8.81 mg hydroxytyrosol/g
trichloroacetic acid (10%) were added to the mixture, which was FW for Kohli variety to 1.45 mg hydroxytyrosol/g FW for Bidhi vari-
then centrifuged at 3000 rpm for 10 min. The upper layer of solu- ety; in the total fruits from 6.97 mg hydroxytyrosol/g FW for Kohli
tion (2.5 ml) was mixed with distilled water (2.5 ml) and a freshly variety to 1.74 mg hydroxytyrosol/g FW for Bidhi variety and in
prepared ferric chloride solution (0.5 ml, 0.1%). The absorbance was the pulps from 3.92 mg hydroxytyrosol/g FW for Kohli to 2.44 mg
measured at 700 nm in a spectrophotometer. Increased absorbance hydroxytyrosol/g FW for Bidhi variety. Total ortho-diphenol con-
of the reaction mixture indicates increase in reducing capability. tent were concentrated differently according to variety: for Kohli
The percentage increase in reducing power was calculated using in peel, for Hamri in total fruit and in pulp for Bidhi variety.
the following equation: Total tannin content (TTC) was found being usually more abun-
dant in Bidhi variety (75.98 mg TAE/g FW in peel, 65.87 mg TAE/g
A test A blank
Increasing in reducing power(%) = 100 FW in pulp and 60.35 mg TAE/g FW in total fruit) than in Kohli and
A blank
Hamri ones (Fig. 6). All differences observed between varieties for
where A test is absorbance of test solution; A blank is absorbance of all samples studied were statistically signicant. For Kohli and Bidhi
blank. Control was prepared in similar manner excluding samples varieties, TTC were concentrated in peel. However in Hamri variety,
without adding standard or test compound. Ascorbic acid was used they were abundant in the total fruit.
as standard at the same concentrations of the samples. Reducing Total anthocyanin content (TAC) was ranged from 429.80 mg
power was measured by varying the concentration of the extract cyanidin-3-glucoside/100 g FW (total fruit) to 162 mg cyanidin-
and the contact time. 3-glucoside/100 g FW (pulp) for Hamri and from 344.89 mg
cyanidin-3-glucoside/100 g FW (pulp) to 144.62 mg cyanidin-3-
2.11. Statistical analyses glucoside/100 g FW (peel) for Bidhi (Fig. 7). Among varieties,
our results showed that Hamri and Bidhi varieties had the low-
For all the experiments three samples of each g juice were ana- est anthocyanin content (p < 0.05). Peel and total fruit of Kohli
lysed and all assays was carried out in triplicate. Data analyses were variety hold both the higher total anthocyanin content with respec-
performed using SPSS software version 22, Duncan multiple range tively 3330.84 mg cyanidin-3-glucoside/100 g FW and 1972.47 mg
test at p < 0.05 probability level. Principal component analysis (PCA) cyanidin-3-glucoside/100 g FW. Our results are similar to those of
was carried out using XLSTAT (2014) for Windows (Addinsoft, New Piga et al. (2005) who indicated that anthocyanins are found mainly
York, USA). in the peel, except for certain types of red fruit, in which they also
occur in the pulp (cherries and strawberries). A signicant differ-
3. Results and discussion ence (p < 0.05) between pulp juice and the other parts juices was
observed only for Kohli variety.
3.1. Phytochemical composition in (peel, pulp, total fruit) g In summary, dark gs in particular, Kohli g (black variety) had
juices of different varieties a signicantly higher content of four phytochemical classes: TPC,
TFC, TOPC and TAC, compared with the green one; with peel being
The phytochemical composition dened by the total polyphe- the major contributing part. TPC, TFC, TOPC and TAC contents were
nol (TPC), total avonoid (TFC), total ortho-diphenol (TOPC), total signicantly different among the three vegetal materials, follow-
tannin (TTC) and total anthocyanin (TAC) contents of peel, pulp ing the order peel > total fruit > pulp for black g and the order total
and total fruit juices from three ripe gs (2nd crop) varieties was fruit > peel> pulp for purple g. Our results are also consistent with
estimated. those of Caliskan and Polat (2011) who reported that some purple
The total phenolic content (TPC) of juices extracts is shown in and black g fruits, from Turkey, contained 2.5-fold higher TPC and
Fig. 3. For the black g, peel juice showed a high TPC, followed by 15-fold higher TAC than the green and yellow ones. Same observa-
total fruit and pulp. Values varied between 50.57 GAE/g FW and tion was shown with Italian g fruits (Del Caro and Piga, 2008) and
74.16 mg GAE/g FW. Concerning purple g, the amount of TPC was Turkish g fruits (Solomon et al., 2006) where black gs were men-
higher and near in all juices, especially for peel and total fruit juices tioned to have higher amounts of polyphenols and anthocyanins
(61.47 mg GAE/g FW and 63.11 mg GAE/g FW.). This may suggest than the green ones and those amounts were concentrated in the
that peel is responsible of the higher content of fruit TPC. How- g peel. The signicant difference between peel and pulp content
ever, for Bidhi variety (green g), amount of TPC was the lowest has also been previously found in other consumed fruits, such as
and close in the three juices (p > 0.05) comparing to other varieties. nectarines, peaches and plums (Toms-Barbern et al., 2001) and
Similar data were reported by Faleh et al. (2012) who found that was mainly related in the anthocyanin content. Anthocyanins are
green varieties of dry g have higher phenolic content than red pigments they impart a pink, red, blue, or purple color in the epi-
ones, but discorded with those founded by Solomon et al. (2006) dermal tissues of owers and fruit. In human diet, they are found
260 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 7. Bar graphics comparing total anthocyanins content (TAC) in juices of different g compartments. Results are expressed as means standarddeviation (n = 3). Bars
with different small letters within one variety are signicantly different (p < 0.05) according to Duncan test. Bars with different capital letters within the three varieties are
signicantly different (p < 0.05) according to Duncan test.

in some cereals, leafy, root vegetables and mostly in fruits (Mazza Table 1
EC50 values obtained in DPPH antioxidant assay of different fruit parts juices of three
and Miniati, 1993).
g varieties with three different phenotypes.
It was proposed that cyanidin was the sole anthocyani-
din skeleton in g fruits (Solomon et al., 2006). Puech et al. Phenotypes Peel (mg/ml) Pulp (mg/ml) Total fruit (mg/ml)
(1975) suggested the presence of three anthocyanins in dark Black 4.52 0.71a 15.45 0.98d 8.63 0.15c
g fruits, namely, cyanidin-3-rhamnoglucoside, cyanidin 3,5- Purple 9.71 0.83c 12.99 0.74d 7.04 0.15b
diglucoside, and pelargonidin 3-rhamnoglucoside, with cyanidin- Green 26.7 1.92e 10.59 0.74c 14.6 0.62d

3-rhamnoglucoside being the predominant pigment in ripe peels. Values are expressed as mean SD (n = 3) of triplicate measurement. Means with
Recently, (Del Caro and Piga, 2008) reported that cyanidin 3-O- different letters are signicantly different (p < 0.05).
rutinoside was present in both peel and pulp of black g, whereas,
cyanidin 3-O-glucoside was dominated in the peel of black g only.
There was a dose-dependent relationship in DPPH scavenging
Different expression of genes controlling the anthocyanin pathway
activity of all three parts (peel, pulp, total fruit) juices of three g
may result in differences in fruit color, with the highest expres-
varieties within the range of concentrations from 2 to 20 mg/ml.
sion associated with the dark varieties. Furthermore, (Oliveira
All samples were proven having antioxidant activities with signi-
et al., 2009) reported the high amount in g peel of the avonoid
cant differences (p < 0.05) between all juices extracts. The peel juice
quercetin 3-O-rutinoside compared to g pulps and leaves.
extract of black g with a mean value of 4.55 mg/ml for EC50 was
Data indicate that chemical composition is dependent on the
almost near to EC50 of ascorbic acid (2.21 mg/ml) (Fig. 8a, Table 1).
fruit part and the variety, thus extracts of darker varieties namely
The total fruit juice extract EC50 of purple variety (mean value
peel, showed higher contents of phytochemicals compared to
6.96 mg/ml) was lower than those of peel (mean value 9.73 mg/ml)
lighter colored extracts.
and pulp (mean value 12.98 mg/ml). The juice extract of the pur-
ple total fruit was found to act as a stronger secondary antioxidant
(Fig. 8b, Table 1). The peel juice extract of green g present the low-
3.2. Antioxidant activity in (peel, pulp and total fruit) juices of est DPPH scavenging activity (Fig. 8c) and the highest EC50 value
different g varieties (Table 1) so that the weakest antioxidant capacity (1214 times
less active than ascorbic acid). Antioxidant activity against DPPH
The antioxidant capacity was evaluated using two commonly was correlated with the concentration, chemical structure, poly-
used colorimetric methods namely, 1,1-diphenyl-2-picrylhydrazyl merization, and degree of antioxidants (Kumaran and Karunakaran,
(DPPH) free radical scavenging activity and reducing power (RP) 2007; Oszmianski et al., 2007).
assay.

3.2.2. Reducing power assay


3.2.1. DPPH radical scavenging activity The reducing capacity of a compound may serve as a signicant
The 1,1-diphenyl-2-picrylhydrazyl DPPH is usually used as a indicator of its potential antioxidant activity. In this assay, the yel-
reagent to evaluate free radical scavenging activity of antioxidants low color of the test solution changes to various shades of green and
(Oyaizu, 1986). In the DPPH assay, the antioxidants were able to blue depending on the reducing power of each compound (Chung
reduce the stable radical DPPH to the yellow colored diphenyl- et al., 2002).
picrylhydrazine. Radical scavengers decolorize the colored DPPH , As shown from Fig. 9, g juices of different parts had effec-
so the loss of absorbance at 517 nm reects radical scavenging tive and powerful reducing power when compared to the standard
activity. ascorbic acid. At 20 mg/ml, peel and total fruit juices extracts of
This study attempted to compare the DPPH free radical (DPPH ) Kohli g, as well as total fruit and peel juices extracts of Hamri g
scavenging activity of different juices of g fruit parts tested (Fig. 8). demonstrated the highest and the nearest absorbance to those of
The scavenging effect was compared to ascorbic acid such as a ascorbic acid at the same concentration. Absorbance values were
standard. The free radical scavenging activity is expressed as per- ranged from 3.36 (Kohli peel) to 2.33 (Kohli total fruit) versus 4.17
centage of DPPH inhibition and by the antioxidant concentration for the ascorbic acid. Differences observed between peel, pulp and
required for a 50% of radical reduction (EC50), so that a lower total fruit of each variety were statistically signicant (p < 0.05)
value of EC50 indicated a higher antioxidant activity and vice versa started from 15 mg/ml. The reducing properties in foods are asso-
(Table 1). ciated with reductones (Duh, 1998; Jayaprakasha et al., 2001). The
A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267 261

phenolic compounds present in g juices may act in a similar studies suggesting that common fruits and vegetables with dark
fashion as reductones by donating electrons and quenching free blue or red colors have the highest antioxidant capacity (Liu et al.,
radicals. 2002; Wu et al., 2006; Celik et al., 2008). Our results are consistent
To conclude, it was found that at the same higher concentration, with those of Solomon et al. (2006) who reported that dark-colored
the extracts cited previously had always the powerful antioxidant gs exhibited the highest antioxidant capacity.
activities, measured either by reducing power test or by DPPH test, Fig varieties with dark peel contain higher levels of polyphenols,
probably because the phenolic compounds in gs react similarly avonoids anthocyanins, and accompanied by higher anti-oxidant
within two methods. Toms-Barbern et al. (2001) suggested the activity compared with g variety with light peel. Peel of black g
fact that the varied radical scavenging activity of extracts depended might be rich sources of natural antioxidants.
on the amount of total phenolic in each fraction. The antioxidant While eating the fruit, consumers tend most often to remove the
capacity is highly correlated with the presence of anthocyanins too peel; however fruit peels are clearly the major source of phenolic
(Shiow and Lin, 2000). The relative contributions of anthocyanins to compounds, acting as antioxidants that should not be discarded; in
the overall antioxidant capacities were estimated in previous study fact, the consumption of total ripe fruits, fresh or as a juice is recom-
to 28 and 36% in dark g fruit (Solomon et al., 2006). mended. A part the presence of antioxidants, g juice is a rich source
Peel of green g, and the pulp of black g, maintain both the of carbohydrates and organic acids (Oliveira et al., 2009), known for
last positions in the antioxidant capacity scale. Black peel holds the their health promoting effects. Its consumption may contribute to
higher antioxidant potential. This study is in agreement with other its protective role against diseases related to oxidative stress.

Fig. 8. DPPH free radical scavenging activity at different concentrations (220 mg/ml) of a reference antioxidant: ascorbic acid and different g parts juices of three varieties
in Tunisia. (a) Kohli, (b) Hamri, (c) Bidhi. Values performed in triplicate.
262 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 9. Reducing power (RP) of different concentrations (220 mg/ml) of a reference antioxidant: ascorbic acid and different g parts juices of three varieties in Tunisia. (a)
Kohli, (b) Hamri, (c) Bidhi. The reducing power was estimated based on the absorbance reading at 700 nm. Values performed in triplicate.

3.3. Changes in total phytochemical composition during fruit to 4.1 mg hydroxytyrosol/g FW (Hamri) for partially ripe fruit. Total
development tannin content values ranged from 45.5 mg TAE/g FW (Kohli) to
134.4 mg TAE/g FW (Bidhi) for ripe fruit and from 14.0 mg TAE/g FW
The phytochemical composition consisting of the total polyphe- (Kohli) to 21.0 mg TAE/g FW (Bidhi) for partially ripe fruit. Results
nol (TPC), total avonoid (TFC), total ortho-diphenol (TOPC), total showed that TTC content in total g fruit was 3 and 6 times higher in
tannin (TTC) and total anthocyanin (TAC) levels was compared ripe g than in partially ripe ones, respectively for Kohli and Bidhi
between 1st crop (partially mature fruit) and 2nd crop (mature varieties, however, the increase is very marked (p < 0.01) in ripe
fruit) gs. Phytochemical composition level increased in all ripe fruit of Hamri variety where TTC achieved an amount of 109.73 mg
fruits compared with partially ripe ones. Results are shown in TAE/g FW.
Fig. 10. Total anthocyanin content in partially ripe fruits was 1150.9 mg
Amounts of polyphenol and avonoid contents show a sig- cyanidin-3-glucoside/100 g FW for Kohli and was approximately
nicant increase (p < 0.05) between two crops. Total polyphenol similar and low in Hamri and Bidhi varieties (respectively
content ranged from 48.0 mg GAE/g FW (Bidhi) to 70.9 mg GAE/g 637.5 mg cyanidin-3-glucoside/100 g FW and 529.8 mg cyanidin-
FW (Hamri) in partially ripe fruit and from 88.5 mg GAE/g FW 3-glucoside/100 g FW). Total anthocyanin content increased, with
(Bidhi) to 153 mg GAE/g FW (Hamri) in ripe fruit. Total avonoid different degrees, in all ripe fruits compared with unripe ones.
content ranged from 6.7 mg CE/g FW (Bidhi) to 9 mg CE/g FW Hamri and Bidhi fruits of 2nd crop were 1.5 times richer in
(Hamri) in partially ripe fruit and from 12.2 mg CE/g FW (Bidhi) anthocyanins than 1st crop fruits. Kohli ripe fruits were 4 times
to 24.7 mg CE/g FW (Hamri) in ripe fruit. A signicant (p < 0.01) richer in anthocyanins than Kohli partially ripe fruits. In fact,
increase in TFC of Kohli variety was shown. Ripe gs are 2 times Kohli variety showed the highest anthocyanin content in ripe
richer in polyphenols than partially ripe ones and 23 times richer fruits (4447.1 mg cyanidin-3-glucoside/100 g FW) with a signicant
in avonoids. increase (p < 0.01) compared to partially unripe gs. However, there
Total orthodiphenol content values ranged from to 3.8 mg was not a signicant difference in anthocyanin amounts between
hydroxytyrosol/g FW (Bidhi) to 16.0 mg hydroxytyrosol/g FW the partially ripe and rip gs of the purple (Hamri) and the light
(Kohli) for ripe fruit and from 0.3 mg hydroxytyrosol/g FW (Bidhi) (Bidhi) varieties were TAC values remain very low (respectively
A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267 263

Fig. 10. Bar graphics comparing total polyphenols content (TPC), total avonoids content (TFC), total tannins content (TTC), total O-diphenols content (TOPC) and total antho-
cyanins content (TAC) between ripe fruit (2nd crop: August crop) and partially ripe fruit (1st crop: July crop) in three g varieties. Results are expressed as means standard
deviation (n = 3).
264 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

Fig. 11. (a) Principal components analysis (scores and loading plots, biplot) based on different phytochemical compounds analyzed in peel juices of three Tunisian g varieties
and their antioxidant activity (%DPPH and reducing power (RP)). TPC: total polyphenols content; TOPC: total O-diphenols content; TFC: total avonoids content; TTC: total
tannins content; TAC: total anthocyanins content. (b) Principal components analysis (scores and loading plots, biplot) based on different phytochemical compounds analyzed
in pulp juices of three Tunisian g varieties and their antioxidant activity (%DPPH and reducing power (RP)). TPC: total polyphenols content; TOPC: total O-diphenols content;
TFC: total avonoids content; TTC: total tannins content; TAC: total anthocyanins content. (c) Principal components analysis (scores and loading plots, biplot) based on
different phytochemical compounds analysed in total fruit juices of three Tunisian g varieties and their antioxidant activity (%DPPH and reducing power (RP)). TPC: total
polyphenols content; TOPC: total O-diphenols content; TFC: total avonoids content; TTC: total tannins content; TAC: total anthocyanins content.
A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267 265

949 mg cyanidin-3-glucoside/100 g FW and 697.1 mg cyanidin-3- The rst PCA (Fig. 11a) accounted 87.65% of the total variance
glucoside/100 g FW). (99.25%), the second PCA (Fig. 11b) accounted 67.49% of the total
The variety (Oliveira et al., 2009) and the maturity stage inter- variance (93.23%) and the third PCA (Fig. 11c) accounted 81.08% of
act between each other to affect fruit properties (Crisosto et al., the total variance (97.74%) on the rst component while the second
2010). Many changes develop during fruit ripening such as, peel component accounted 16.68%.
colour, antioxidant capacity (Toor and Savage, 2005) and physic- Comparisons between PCAs plots indicated that for three PCAs,
ochemical properties (Alkarkhi et al., 2011) in particular acidity PC1 was dominated by the following variables: TAC, TOPC, TFC and
decrease (Wu et al., 2007; Crisosto et al., 2010; Zhang et al., 2010), TPC that were correlated positively with Kohli and Hamri varieties
sugar increase (Wu et al., 2007) and aromatic composition (Trad and so they were the mainly responsible for the discrimination of
et al., 2012; Braga et al., 2013), therefore the production of phy- dark peels. However, Bidhi group (green variety) was negatively
tochemicals is also inuenced. Total phenolic (Josefa et al., 2006) associated with PC1 and positively with PC2 and was characterized
and total anthocyanin (Shiow and Lin, 2000) contents were shown by the abundance of tannins.
increased in ripe fruits. However, the present results are not consist Reducing power and DPPH groups were correlated positively
with those of Kubola and Siriamornpun (2011) who mentioned that with Kohli and Hamri groups for peel and total fruit PCAs with a
fruit total phenolic and total avonoid contents decreased during slightly higher correlation for Kohli variety (Fig. 11a and b). Antho-
the fruit development stage. cyanin, avonoid and polyphenol, concentrated in Kohli variety
Fruit ripening process is always accompanied by a change in more than in Hamri one, seem to be the principal contributors to
fruit softening and texture. Enzymes are shown to have a role in strong the antioxidant activity revealed by the reducing power and
fruit ripening. Expression of enzymes involved in the degradation %DPPH scavenging activity. However, for PCAs pulp, RP and DPPH
of many different cell wall polymers present in different g tissue is were correlated negatively with PCA1 (Fig. 11c). Tannins provided
coordinated both in time and amount with the fruit development by green gs were apparently responsible of the antioxidant capac-
(Owino et al., 2004). Peroxidase, polyphenol oxidase (PPO), pro- ity of g pulps. Tannins are well known as potent antioxidants.
tease and carbohydrases are involved in mango peel ripening (Ajila The soluble tannins are gradually converted into non-soluble con-
et al., 2007). densed form as the fruit begins to ripen and advances progressively
Differences in phytochemical content between the two crops (Myhara et al., 1999).
can be explained by weather conditions too. At last of August, Chemometric observations were consistent with those obtained
when 2nd crop was picked, environment was more warm, dry and during the evaluation of antioxidant activity of juices. The principal
sunny than at the beginning of July (1st crop), and so, was favor- component analysis gave further information about the differences
able for fruits growth and development. The sun-exposed peel of among the g parts as well as their implication on the antioxidant
apples terminal fruit had higher anthocyanin levels than shaded activity revealed by the reducing power and %DPPH scavenging
peel (Awad et al., 2000). Results were in accordance with those of activity. Results clearly indicated that each variety could be distin-
Veberic et al. (2008) for gs varieties from northern Mediterranean guishable from the other. Phytochemical compounds accumulate
region who stated that the sun-shining weather in August is more differently depending on the fruit part and the variety.
favorable for gs growth than in September which is marked by
cooler and moister weather. However, phenolic concentration lev-
els reported were several times higher than those noticed in the 4. Conclusion
present study. This could be explained by the difference of vari-
ety, climate and environment, as Tunisia is located in the south This is the rst study comparing juices of F. carica peels, pulps
Mediterranean region. The inuence of the region of cultivation and total fruits, contributing to more knowledge about the nutri-
(north or south) on the concentration of phenolics in bananas was tional aspects of an important fruit of the Mediterranean diet.
conrmed (Mndez et al., 2003). The level of anthocyanin in the The content level of phytochemicals (TPC, TFC, TOPC, TTC, and
fruit depends on various factors, namely: species, varieties, growing TAC) is usually inuenced not only by the variety, but also varies
conditions, seasonal variations, maturity index, processing meth- signicantly from one fruit part to the other. Antioxidant capacity
ods, and storage conditions (Melgarejo et al., 2000; zkan, 2002). In of g seemed to be mostly related to the peel part and not the
contrast, Vallejo et al. (2012) mentioned that g fruit from a crop in pulp part. Facts suggest that in a general way, the peel color allow
(MayJune) showed even further highest values of total phenolics distinguishing the fruit phenol and anthocyanin contents. The large
comparing to a second crop in (AugustSeptember). However, this amount of tannins contained in different compartments of green g
difference is signicant in peels and not in the pulps of g fruit. may cause its non-negligible antioxidant capacity.
In general way, during the ripening period, weather conditions The phytochemical composition of g including phenols,
could be either favorable or stressful for the fruit growth. Pro- avonoids, ortho-diphenols tannins and anthocyanins contents is
duction of avonoids, classied as environmental compounds inuenced by the ripening stage and varieties of g.
because of their production in direct response to environmental Total polyphenol, total avonoid, total ortho-diphenol, total tan-
conditions, is dependent on ultraviolet light and CO2 levels (Daniel nin and total anthocyanin contents can be used as indicators of the
et al., 1999; Caldwell et al., 2005). antioxidant activity of foods.
Results of this study would stimulate further researches on dark
gs, especially; g peel, which is a by-product, to be utilized a useful
3.4. Chemometric analysis source of natural food preservative from a nutritional related point
of view and other g parts as a potential new source of natural
The chemometric analysis results generated three biplots show- antioxidants for food and pharmaceutical industries.
ing groupings and subgroupings: the principal component analysis
(PCA) (Fig. 11) was carried on the data to compare the phytochem-
ical composition of peels (Fig. 11a), pulps (Fig. 11b) and total fruits Acknowledgments
(Fig. 11c) juices of three studied varieties of gs and to identify
the factors inuencing each one. The position of each variable in This study was supported by a grant (to Arij Harzallah) from
the loading plot describes its relationship with the other variables. MOBIDOC device launched under the Supported Project to the
Variables that are close to each other have high correlations. research and Innovation System (PASRI), funded by the European
266 A. Harzallah et al. / Industrial Crops and Products 83 (2016) 255267

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