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Antioxidant Activity Analysis of Opuntia Species as Influenced by Season and

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DOI: 10.11623/frj.2020.28.2.02

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Flower Res. J. (2020) 28(2) : 60-68 ISSN 1225-5009(Print)
DOI https://doi.org/10.11623/frj.2020.28.2.02 ISSN 2287-772X(Online)

O R IG IN A L A R T IC L E

Antioxidant Activity Analysis of Opuntia Species as Influenced by

Season and Plant Parts
Eun Ha Oh1†, Raisa Aone M. Cabahug2†, Young Jin Choi1, and Sang Yong Nam1,2*
1
Department of Environmental Horticulture, Sahmyook University, Seoul 01795, Korea
2
Natural Science Research Institute, Sahmyook University, Seoul 01795, Korea
†
These authors have contributed equally

Received 3 December 2019; Revised 6 March 2020; Accepted 8 April 2020

Copyright © 2020 by The Korean Society for Floricultural Science

Abstract The prickly pear cactus (Opuntia), native to
Mexico, has grown in popularity and is locally grown and
adapted on Jeju Island. The fruits of this cactus species are
in particular widely employed as raw materials, which are
then processed into various food and medicinal items,
including chocolates and vitamins, for purposes of human
consumption. Because this crop has been dubbed one of
Jeju’s iconic agricultural crops, research studies elucidating
the prickly pear cactus’ medicinal properties, including
antioxidant activity, of this particular plant and related
cultivated species have demonstrated high value to the
scientific community. Currently, consumers do not purchase
products for consumption alone, but in addition for their
added health benefits. The present study in particular honed
in on two species of prickly pear cactus that are cultivated
on Jeju Island which include: ‘Baeknyeoncho’ (Opuntia
ficus-indica) and ‘Cheonnyeoncho’ (Opuntia humifusa). From
these species, specific plant parts including the flower,
mature and young stems, roots, and fruit were subjected
to further antioxidant analysis, which included the
determination of polyphenol, flavonoid, DPPH radical, ABTS
radical, and anthocyanin levels. These particular antioxidants
were determined during two seasons, over the course of the
summer and winter. Results revealed that the antioxidant
activity for both species was more active during the summer
season. Antioxidant levels occurred at the highest rates
within the flowers of the cactus plants. However, of
significant note was that the cactus stem, in both mature
and young plants, possessed higher antioxidant activity
*Corresponding author: Sang Yong Nam
Tel: namsy@syu.ac.kr
E-mail: +82-2-3399-1732
ORCID: https://orcid.org/0000-0002-4351-447X
compared to those of the fruit that is currently employed
for commercial purposes.
Additional key words: ABTS radicals, anthocyanin, DPPH,
flavonoid, polyphenol, prickly pear cactus, succulents
Introduction
There are many economically promising plants that belong
to the Cactaceae family. The most popular of which is Opuntia
(Russell and Felker 1987). Opuntioid cacti, also known as
prickly pear cacti, is characterized as a succulent plant with
a shallow root system, swollen stem structure, thick and waxy
cuticle, which allows water storage in its organs (Anderson
2001; Ogburn and Edwards 2010). These plants are energy
efficient and are able to survive in drought due to their use
of the Crassulacean Acid Metabolism (CAM) which allows
plants to intake atmospheric CO2 during night time to
minimize water loss (Erwin 2009; Taiz and Ziger 2010). These
cacti have been cultivated in the Mediterranean region as well
as in Southeast Asia and are used as ornamental plants, food
crops and a source of raw materials for pharmaceutical (Butera
et al. 2002; Kim et al. 2012).
Especially in Korea, prickly pear cactus is famously
cultivated in Jeju Island where they are grown rapidly for its
economic demand as a key component for healthy products
such as chocolates, cookies, tea, jam, juice, vitamins and other
supplementary drugs (Ahn 1998; Gonzalez-Stuart and Rivera
2019; Jung et al. 2013; Lopez 1995). Because of its importance
in human consumption and medicine, breeders have tried to

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Flower Res. J. (2020) 28(2) : 60-68
analyze its phenotypic and genetic characteristics to enhance
its species such as that of ‘Baeknyeoncho’ (Opuntia ficus-indica)
(In et al. 2006; Mazri 2018) and ‘Cheonnyeoncho’ (Opuntia
humifusa) (Srikanth and Whang 2015) and increase its production
through tissue culture (Al-Khayri et al. 2018; Pérez-Molphe-
Balch et al. 2015).
Numerous studies have continued to identify its chemical
composition in the different parts of these succulent species.
‘Baeknyeoncho’ has been studied in terms of chemical
characterization of its chemical composition and anti-oxidant
properties from its fruit (Butera et al. 2002; Gralati et al.
2003), flowers (Ammar et al 2012; Benayad et al. 2014),
stems or cladodes (Lee et al. 2003; Ramirez-Moreno et al.
2013). Likewise, ‘Cheonnyeoncho’ species are also studied
for similar chemical composition and antioxidant properties
using their fruits (Cha et al. 2013), cladodes (Jun et al.
2013) and other plant parts (Jung et al. 2011).
These related studies pave the way for medical researchers
to be able to use this data in order to determine its medical
benefits. Several studies have been conducted identifying its
effect and its ability to be a potential cure or prevention for
numerous medical conditions such as gastric lesions (Kim et
al. 2012), cardiovascular diseases (Han et al. 2012), chronic
diseases, diabetes, obesity and cancer (Diaz et al. 2017),
etc.
Currently, the most common source for its consumption
and use as a raw material is the fruit. To this day, domesticated
species has been researched and bred to produce enhanced
fruits with respect to size, shape, texture, flavor and
antioxidant benefits (Ingles et al. 2002; Reyes-Aguero and
Rivera 2011; Tesoriere et al. 2004). Opuntia species fruits were
found to have protein (4.70 - 11.6%), fat (0.69 - 1.25%), crude
fiber (5.9 - 50.3%), ash (2.0 - 15.10%), as well as phenolic
acids (33.40 - 56.80%) and flavonoids (16.80 - 19.40%) (Diaz
et al. 2017).
Numerous studies show that antioxidant activities are
affected by change in certain factors such as atmospheric gases
(Piga et al. 2003; Teissedre et al. 1996), relative humidity (Shin
et al. 2007), but among several factors temperature (Cordenunsi
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61
et al. 2005; Reblova 2012) has been more prominent. In respect
to the demand of Opuntia, there are only a few studies that
determine the difference of antioxidant activity towards its plant
organs, species, and the season of harvest. Hence, this study
aims to determine these factors affecting antioxidant activity
among the two common species of Opuntia in Korea, which
are ‘Baeknyeoncho’ and ‘Cheonnyeoncho’.
Materials and Methods
Plant Materials
Two species of the prickly pear cactus were used namely:
‘Baeknyeoncho’ and ‘Cheonnyeoncho’ (Fig. 1) which were
taken from Jeju Island. These samples were taken to the
Physio Lab, Department of Environmental Horticulture, Sahmyook
University, Seoul.
Experimental Design
The study was conducted using a 5 x 2 factorial arrangement
in Completely Randomized Design (CRD) for each species
and antioxidant component investigated in this study. Each
analysis was replicated five times. The respective parts that
were harvested from each species served as Factor A which
were the flower, mature and young stems, roots and fruit.
The same plant parts were harvested for two separate seasons
which served as Factor B, summer (August) and winter
(December).
Antioxidant Analysis
Different extraction and protocols to determine the levels
of polyphenol, flavonoid, DPPH radical, ABTS radical, and
anthocyanin were followed from previously published
studies, and are indicated below. For content analysis, a
modified Folin-Ciocalteau method was followed as indicated
by the study of Hwang et al. (2015). The ballic acid was
dissolved with distilled water and served as a standard
solution. A 0.5 mL extract (1 mg·mL-1) was mixed with
0.5 mL of the polyin reagent and was lent to reacted at
room temperature for 3 min. The specimen was prepared
using 95% ethanol to make a 1mL extract of the specimen.
62
Fig. 1. Jeju Island prickly pear cactus species: A. ‘Baeknyeoncho’;
and B. ‘Cheonnyeoncho’, and the different plant parts used in the
study to analyze antioxidant activity: 1. flower; 2. mature stem; 3.
young stem; 4. fruit; and 5. roots.
Polyphenol and Flavanoid Content Analysis
Na2CO3 at 2% was added to the sample extract in order
to create a total volume of 1.5 mL and was mixed for 2
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Flower Res. J. (2020) 28(2) : 60-68
hours (Gutfinger 1981; Hwang et al. 2015). At 760 nm
absorbance, the absorption degree (OD) was measured
using a microplate reader (Infinite M200 Pro, Techan Group
Ltd., San Jose, CA, USA). The total polyphenol content
contained in the specimen is expressed as the Total Acid
Equivalent (GAE) per gram of specimen through a standard
curve of colic acid (6.25 - 100 μg·mL-1).
Similar methods were employed, but the total flavonoid
content was obtained using quercetin (Sigma-Aldrich, USA)
and was measured the absorbance at 415 nm (Chon et al.
2012; Lister et al. 1994).
DPPH Radical
DPPH (22-diphenyl-1-picrylhydrazyl) radical dissipation
was measured according to the DPPH free radical removal
method (Jang et al. 2015). After adding a specimen extract
to the DPPH solution, it was dissolved in methanol. This was
measured and marked with Trolox equivalent (TE) having
1 g in fresh weight. 1 mL of a specimen solution was added
to a 3 mL of 60 μM 1-1-diphenyl-2-picryl-hydrazyl (DPPH)
and was vortexed. After 15 min at room temperature, the
absorbance was measured at 517 nm. After dissolving vitamin
C (ascorbic acid) in EtOH, a standard solution was prepared.
A 50 μM of DPPH solution was prepared in EtOH. The
absorbance value of the DPPH solution was measured using
the microplate reader. Antioxidant capacity (%) was obtained
by using the formula: 100 - 100*(absorbance value of sample
- blank absorbance value) / control's absorbance value -
blank's absorbance value.
ABTS Radical
ABTS (2-azinobis-3-ethylbenzo-thiazoline-6-sulfonic acid)
radical dissipation was measured by the method (Re et al.
1999). After mixing 2.45 mM potassium permulate and 7
mM ABTS solution in a ratio of 1:1(v/v), the ABTS solution
was set aside for 12 - 16 hours and diluted with methanol.
The absorbance was set at 734 nm and was measured after
adding 3 mL of an ABTS solution to a 0.3 mL extract and
leaving let it sit for 6 min. The results are expressed in TE
and 1 g of fresh weight.
Flower Res. J. (2020) 28(2) : 60-68 63

Anthocyanin Content Analysis
The total anthocyanin content was measured by the method
of Pantelidis et al. (2007). It was calculated by using this
-1
formula: Contents of total anthocyanin (mg·g ) = [(A × MW
× 103 × dilution factor)]/ε. Where: A = (A 520-A 700) pH
1.0-(A 520-A 700) pH 4.5; ε = molar extension coefficient
for cyaniding-3-glucoside (26,900); MW = molecular weight
-1
of cyanidin-3-glucoside (449.2 g·mol ). The absorber 510
nm was measured and the buffer solution pH 1.0, pH 4.5
was used.
Data Analysis
Statistical analyses were conducted using Statistical
Product and Service Solutions for Windows, version 16.0
(SPSS Inc., Japan). The data were analyzed using analysis
of variance (ANOVA), and the differences between the
means were tested using t-test and Duncan’s multiple range
test (p < 0.05).
Results and Discussion
Previous studies suggest that antioxidant levels vary between
species and cultivars (Allaith 2018). This was likewise observed
for comparative studies of antioxidant levels between varieties
for apples (Wpjdylo et al. 2008), garlic (Chen et al. 2013),
onion (Lisanti et al. 2016), grapes (Singha and Das 2014) and
purslanes (Lim and Quah 2007) among others. A similar study
was conducted by Abdel-Hameed et al. (2014) of two prickly
pear cactus species were analyzed for their antioxidant,
phytochemical and nutritional properties. However, the species
were not properly identified and were just tagged as red and
yellow cactuses. Pertaining to the Korean species used in
the study, ‘Baeknyeoncho’ possesses reddish colors, while
‘Cheonnyeoncho’ is prominently yellow. Similar results were
also reported by the said study having red cultivars with higher
total phenolic properties compared to the yellow cultivars.
‘Baeknyeoncho’ indicated higher contents of polyphenol
(7.04 μg·mL-1) and anthocyanin (0.26 μg·mL1). Studies of
Briedis et al. (2003) suggests that there is a correlation
between high antioxidant activity with high polyohenol
content. Intake of food with high polyphenol content

The results of the study are presented and expounded promotes better nutrient absorption, improves metabolism,

based on their cultivar, season and plant part, and their and decreases inflammation in both human and animal

respective antioxidant activity. A comparison of means was models (Bolca et al. 2003; Cheynier et al. 2015).

likewise done. Discussions and literature that provide ‘Cheonnyeoncho’ species had a higher flavonoid (7.34 μ

probable cause of the results are elucidated.
Opuntia Species
Table 1 presents the antioxidant activity of two species of
Opuntia. Results indicated that species were highly affected
(p < 0.001) by antioxidant activity of polyphenols, flavonoids,
ABTS radical and anthocyanin. On the other hand, DPPH
radical results were statistically non-significant (p > 0.659).
g·mL-1) and ABTS radical (6.53 μg·mL1) content. Despite
having no significant differences, DPPH radical was found to
be higher in ‘Cheonnyeoncho’ species compared to those of
‘Baeknyeoncho’. This results was also similar to those of the
studies of Lee et al. (2006). It was found that the increase
of ABTS and DPPH radicals were observed with higher
flavonoid content in Chinese mulberries. This may be
attributed to their same chemical property of hydrogen- or

Table 1. Antioxidant activity of two prickly pear cactus cultivars ‘Baeknyeoncho’ (Opuntia ficus-indica) and ‘Baeknyeoncho’ (O. humifusa).
Antioxidants (μg·mL-1)
Cultivar
Polyphenol Flavonoid DPPH radical ABTS radical Anthocyanin
z
‘Baeknyeoncho’ 7.04 ± 1.49 4.45 ± 1.36 3.41 ± 0.38 6.18 ± 0.30 0.26 ± 0.12
‘Cheonnyeoncho’ 5.82 ± 1.70 7.34 ± 2.22 3.45 ± 0.43 6.53 ± 0.42 0.09 ± 0.12
F-test y ** ** NS ** **
z
Mean ± SD.
y
NS, *, **, Non-Significant or significant at p = 0.05 or 0.01, respectively.

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64
electron-donation to flavonoids. Flavanoiids are compounds
that are known to fight off allergens, pathogens, biruses and
prevents cardiac problems, eye disorders, cancers and even
Alzhimer’s (Shahidi and Ambigaipalan 2015; Vodnar et al.
2017).
Season
An important factor that majorly affects plants, its
mechanisms, and as well as the important compounds
produced within (Went 1953). Investigating how seasonal
harvesting of plants has been found to be very important
especially in high-valued crops wherein certain chemical
compositions or compounds are centers of interest.
Differences in seasonal harvest significantly affected the
antioxidant levels of Opuntia (p < 0.000). A comparison of
means suggested that the different seasons were highly
different for antioxidants polyphenol, flavonoid, DPPH radical
and anthocyanin (Table 2a). Non-significant differences
between seasons were observed from only those of ABTS
radical. Higher antioxidants were significantly taken from
those harvested during the summer season. Even those for
ABTS radical that was found to be non-significant showed
a higher antioxidant level during the summer season
compared to those of the winter season. Results were similar
when antioxidant activities were analyzed between groups of
Opuntia species (Table 2b).
Studies showed that this was particularly observed through
several crops on their antioxidant activity (Reblova 2012).
Almeselmani et al. (2006) explained that antioxidant levels
increase during high-temperature stresses, like the summer
season, in plants as a protective mechanism to withstand
damage to plant cells. This was evident in the study of
Table 2. Antioxidant activity of prickly pear cactus in response to seasons.
Antioxidants (μg·mL-1)
Season
Polyphenol Flavonoid
z
Summer 7.11 ± 1.71 6.67 ± 2.69
Winter 5.75 ± 1.41 5.11 ± 1.61
F-test y ** **
z
Mean ± SD.
y
NS, *, **, Non-Significant or significant at p = 0.05 or 0.01, respectively.
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Flower Res. J. (2020) 28(2) : 60-68
Wang and Zheng (2001) with strawberries, wherein plants
that were grown in cooler temperatures had the lowest
phenolic acid, flavonoids, and anthocyanins while those of
high-temperature growing conditions yielded the highest
phenolic content and radical absorbance capacity. Aside
from the growing conditions, temperature during extraction
temperatures has the same effect as observed among grapes
(Spigno et al. 2007).
Plant Parts
Different plant parts of succulents are edible and may be
used for different purposes. As an integral ingredient and
raw material for several commercial products, it would be
best to identify the highest component of beneficial
antioxidants and their activity within different plant parts of
Opuntia species. Hence, different plant parts were analyzed
for their antioxidant activity.
Results revealed that the different plant parts were
significantly affected by the antioxidant activity (p < 0.001)
(Table 3a) regardless of the species. Among these plant parts,
flowers were found to have the highest antioxidant activities
while those of the fruits were found to have the lowest
antioxidant activities except for the DPPH and ABTS radical.
It could be noted that there was a higher antioxidant activity
level for those of the stems (young and mature) compared
to the fruits. Likwise, it was observed that within Opuntia
species ‘Baeknyeoncho’ and ‘Cheonyeoncho’ had similar
results (Table 3b). Despite having the least antioxidant activity,
fruits are surprisingly more commonly and commercially used
among plant part of prickly pear cactuses for processing foods
and other by-products (de Cortazar and Nobel 1992; FAO
2013). These flowers with high antioxidant contents may be
DPPH radical ABTS radical Anthocyanin
3.71 ± 0.34 6.43 ± 0.36 0.25 ± 0.16
3.15 ± 0.23 6.28 ± 0.44 0.11 ± 0.09
** NS **
Flower Res. J. (2020) 28(2) : 60-68 65

Table 3. Antioxidant activity of ‘Baeknyeoncho’ (O. ficus-indica) and ‘Baeknyeoncho’ (O. humifusa) in response to seasons.
Antioxidants (μg·mL-1)
Opuntia species Season
Polyphenol Flavonoid DPPH radical ABTS radical Anthocyanin
z
‘Baeknyeoncho’ Summer 7.82 ± 1.04 4.42 ± 1.39 3.75 ± 0.18 6.25 ± 0.31 0.35 ± 0.10
Winter 6.26 ± 1.47 4.47 ± 1.37 3.07 ± 0.11 6.10 ± 0.28 0.18 ± 0.06
‘Cheonyeoncho’ Summer 6.40 ± 1.96 8.93 ± 1.49 3.67 ± 0.45 6.60 ± 0.32 0.15 ± 0.15
Winter 5.24 ± 1.16 5.75 ± 1.61 3.23 ± 0.11 6.47 ± 0.44 0.05 ± 0.12
z
Mean ± SD.

Table 4. Antioxidant activity of prickly pear cactus in response to plant parts.

Antioxidants (μg·mL-1)
Plant parts
Polyphenol Flavonoid DPPH radical ABTS radical Anthocyanin
z
Flower 8.91 ± 0.89 7.32 ± 0.88 4.12 ± 0.09 6.91 ± 0.24 0.36 ± 0.18
Mature stem 6.84 ± 1.70 5.41 ± 1.76 3.41 ± 0.37 6.26 ± 0.15 0.21 ± 0.11
Young stem 6.31 ± 1.44 6.52 ± 2.93 3.32 ± 0.30 6.24 ± 0.24 0.17 ± 0.15
Root 5.18 ± 0.76 5.43 ± 2.11 3.28 ± 0.27 6.22 ± 0.20 0.13 ± 0.09
Fruit 5.88 ± 1.37 5.09 ± 2.89 3.30 ± 0.41 6.51 ± 0.80 0.06 ± 0.06
y
F-test ** ** ** ** **
z
Mean ± SD.
y
NS, *, **, Non-Significant or significant at p = 0.05 or 0.01, respectively.

Table 5. Antioxidant activity of ‘Baeknyeoncho’ (O. ficus-indica) and ‘Baeknyeoncho’ (O. humifusa) in response to seasons.
Antioxidants (μg·mL-1)
Opuntia species Plant parts
Polyphenol Flavonoid DPPH radical ABTS radical Anthocyanin
z
‘Baeknyeoncho’ Flower 8.16 ± 0.43 6.55 ± 0.47 4.04 ± 0.06 6.74 ± 0.15 0.45 ± 0.08
Mature stem 8.43 ± 0.60 4.54 ± 0.66 3.39 ± 0.25 6.27 ± 0.15 0.28 ± 0.06
Young stem 7.60 ± 0.70 4.70 ± 0.94 3.36 ± 0.28 6.10 ± 0.19 0.28 ± 0.13
Root 5.75 ± 0.52 4.07 ± 1.24 3.41 ± 0.33 6.08 ± 0.12 0.21 ± 0.06
Fruit 5.63 ± 0.59 2.39 ± 0.18 2.92 ± 0.04 5.77 ± 0.19 0.11 ± 0.92
‘Cheonyeoncho’ Flower 9.66 ± 0.41 8.08 ± 0.28 4.20 ± 0.03 7.09 ± 0.18 0.26 ± 0.22
Mature stem 5.25 ± 0.39 6.27 ± 2.10 3.44 ± 0.47 6.24 ± 0.15 0.14 ± 0.11
Young stem 5.02 ± 0.39 8.35 ± 3.13 3,28 ± 0.33 6.38 ± 0.20 0.05 ± 0.05
Root 4.61 ± 0.47 6.79 ± 1.93 3.15 ± 0.07 6.35 ± 0.17 0.05 ± 0.37
Fruit 7.12 ± 0.16 7.80 ± 0.71 3.69 ± 0.06 7.24 ± 0.26 0.00 ± 0.00
z
Mean ± SD.

used for raw materials if functional foods, medicine, flavorings
and key ingredients for commercial products. Studies of
Cavaiuolo et al. (2013) reported that flowers are natural
sources of bioactive compounds and the high concentration
of antioxidants sparks from the high flower pigments, such
as carotenoids and polyphenols, on their petals.
Aside from the flowers, the use of stems has also proved
to be better source of antioxidant activity in contrast with the
fruits. Studies on grape stems had similar results to those of
prickly pear cactus where their stems had significant amounts
of polyphenolic compounds like phenolic acids and flavonoids
(Souquet et al. 2000). Because Opuntia species are succulents,
most of the most important physiological processes are found
within their cladodes. These stems do not primarily grow for
support, but they are enlarged storage units for the whole
plant (Andersen 2001). Hence, it may not be suprising that
antioxidants are found within these organs. Several crops are
found to have high antioxidant levels in their leaves such
as that of Cassua spp. (Kaur et al. 2006; Kumaran and
Karunakaran 2007; Siddhuraju et al. 2002), peony (Li et al.

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66
2009), Nasturium (Garzon and Wrolsyan 2009) among others.
Acknowledgement
This work is supported by Succulents Export Innovation
Model Development towards Chinese Market (514006-03-1-HD040)’,
Ministry of Agriculture, Food and Rural Affair and Sahmyook
University Research Fund.
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