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Núñez-Gastelum et al., 2018
JPACD 2018 (20): 23-33
23
Morphological characteristics, chemical composition and
antioxidant activity of seeds by four wild Opuntia species from
North of Mexico
José Alberto Núñez-Gastélum
1
, Raquel González-Fernández
1
, Arlette Hernández-
Herrera
1
, Olga Nydia Campas-Baypoli
2
, Roberto Rodríguez-Ramírez
2
, Naun Lobo-Galo
1
,
José Valero-Galván
1*
1
Departamento de Ciencias Químico-Biológicas, Instituto de Ciencias Biomédicas,
Universidad Autónoma de Ciudad Juárez, Anillo envolvente del PRONAF y
Estocolmo s/n, Ciudad Juárez, Chihuahua, 32310, México.
2
Departamento de Biotecnología y Ciencias Agroalimentarias, Instituto Tecnológico
de Sonora, 5 de febrero 818 sur, Ciudad Obregón, Sonora, 85000, México.
*
Corresponding author: jose.valero@uacj.mx
Received: November 7, 2017; Accepted: April 9, 2018.
ABSTRACT
Morphological characteristics and chemical composition of seeds of four species of Opuntia
genus endemic to the Samalayuca Valley were evaluated in this study. Morphology and
chemical composition of the four species were clearly different. Seeds of O. polyacanta var.
arenaria presented the highest values of area, length and width. However, O. phaeacantha
showed the highest values in palmitoleic acid (1.34 ± 0.12%), stearic acid (5.60 ± 0.47%), oleic
acid (19.42 ± 1.04%), alpha linolenic acid (2.42 ± 0.33%), arachidic acid (0.61 ± 0.11%), and
eicosenoic acid (1.74 ± 0.36%); but, this species showed the lowest values in linoleic acid
(54.35 ± 2.91 %) content. In conclusion, seeds of O. phaeacantha could be an important new
source of health-promoting polyunsaturated fatty acid, and its use in arid and semi-arid regions
should be encouraged.
Keywords: Morphological seed, Chemical composition, Opuntioideae, fatty acids, antioxidant
capacity.
INTRODUCTION
The Opuntia genus of plants is native to the American continent. Species of this genus are
found to grow naturally at different altitudes, climates, and level of annual precipitation in this
continent (Rebman and Pinkava, 2001; Reyes-Aguero et al., 2006). In Mexico, 84 Opuntia
species have been reported to this date, but little is known about these weakly protected
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JPACD 2018 (20): 23-33
24
species despite their significant commercial potential and environmental impact (Illoldi-Rangel
et al., 2012). Opuntia genus are dominant components of natural vegetation of the Chihuahuan
Desert and these species contribute to the diet of insects, birds and mammal species
(Mandujano et al., 1997; Montiel and Montaña, 2000; Soberon et al., 2001).
Furthermore, they are also used as source of forage, raw and food material by local
communities. Morphology and chemistry composition of seeds has been well characterized in
the case of the commercial Opuntia ficus-indica specie (Rebman and Pinkava, 2001; Özcan
and Juhaimi, 2011 Chougui et al., 2013). However, the nutritional value of seeds from other
Opuntia species growing under natural conditions has been only partially investigated. Previous
reports have specified that cladodes, seed and pulp of Opuntia genus were rich in oleic, palmitic
and linolenic acids, while the fruits constitute an important source of functional compounds,
including pigments (carotenoids and betalains), vitamins and minerals (Kuti, 2004; Guevara-
Figueroa et al., 2010). These compounds have been further examined for their contribution to
a healthy human diet and also as ingredients for the design and development of new foods
(Saenz et al. 2004). Recently, fruits of these species have also been examined for their reported
medicinal properties, showing several benefits as hepatoprotective, preventing or treating
anemia, as well as antinflammatory, antihyperglycemic and hypocholesterolemic effects
(Sanyal et al. 2015; González-Ponce et al., 2016; Jung-Woo et al., 2016: Ondarza, 2016).
The morphological study of Opuntia seeds contribute to the taxonomic information of the
different species. However, in the consumption of the fruits of Opuntia, as well as in the
preparation of some juices, the seeds constitute a waste. Therefore, local Opuntia species
seeds could constitute an important new source of fatty acids, nutritional vitamins, polyphenols,
flavonoids, tannins, natural antioxidants and oil. Yet to date, no proximal composition,
antioxidant activity, phenolic content and fatty acids of seed of Opuntioideae for Northern
Chihuahuan Desert has been published. In this study, the morphometric and chemical
characterization of the seeds of some species of Opuntia located in Samalayuca area of the
state of Chihuahua, Mexico, have been analyzed.
MATERIAL AND METHODS
Reagents
Methylene blue, Folin-Ciocalteu reagent, Na
2
CO
3
, K
2
CO
3
, gallic acid, 2,2-diphenyl-1-
picrylhydrazyl (DPPH), TROLOX, Na
2
SO
4
,
and were acquired from Sigma (St. Louis, MI, USA).
Ethyl ether, toluene, and methanol were purchased from J. T. Baker S. A. de C. V. (Estado de
México, México). Fatty acids standards FAME MIX C8-C22 were purchased from Supelco
(Bellefonte, PA, USA). HCl was obtained from Monterrey Chemistry Products (Monterrey,
Nuevo León, México).
Plant Material
Opuntia fruits were sampled in Samalayuca Medanos Valley, area situated at 50 km south of
Juarez City, Chihuahua State, Mexico (31°39’36’’ - 29°25’12’’ North Latitude and 109°02’24’’ -
107°14’24’’ West Longitude). The area has been described as a very dry ecosystem with an
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JPACD 2018 (20): 23-33
25
annual average temperature of 12–18°C, and at present, an annual precipitation is 200–400
mm. Plants of O. engelmannii, O. polyacantha var. arenaria, O. macrocentra, and O.
phaeacantha were randomly collected, with 20 m apart from each other. Twenty undamaged
and homogeneous fruits from individual plants per specie were collected, based on their
presentation of maximum fruit maturation. Fruits were stored in an airtight polyethylene bag
and immediately transported to the laboratory of the Universidad Autónoma de Ciudad Juárez.
All samples were lyophilized (Labconco freeze dry/shell freeze system, Labconco Corp.,
Kansas City, MO), milled in a Nutribullet household mixer (Nutribullet, LLC, USA), and stored
at −80°C.
Morphological Analyses
Ten fruits per specie were used for weight and size determination (Photograph 1). To examine
the seed characteristics, seeds were separated from the juicy pulp, washed thoroughly with
distilled water, and then dried and stored in paper bags at ambient temperature until further
analysis. Seeds (20 units per specie) were used for size and weight determinations. Seed
weight was determined in an analytical balance (Mettler Toledo AJ150, Ciudad de México,
México). Then, seed were digitally photographed under a stereomicroscope, and the images
were studied using image analysis software (ImageJ, Bethesda, MD, USA) to obtain qualitative
and quantitative data. External properties such as area, length and maximum diameter of seed
were measured according to the procedures proposed by Guerrero-Muñoz et al. (2006).
Internal structures of seeds were characterized under the microscope to determine the seed
coat and the funicular envelope composition of hard seeds of these species. Ten healthy seed
were immersed for 4 days in methylene blue. Seeds were scarified with a knife by making a
longitudinal cuts and internal structures such as embryo plus cotyledon and coat areas were
measured according to the procedures proposed by Guerrero-Muñoz et al. (2006).
Chemical Analyses
All the proximate analyses were determined on three analytical replicates and were determined
in concordance to the AOAC (2006). Moisture percentage content was measured by
evaporation at 130°C for 2 h (AOAC, 930.15). The total protein content was obtained by the
total nitrogen quantified by the Kjeldahl method (AOAC, 992.15). The ash content was
calculated by the incineration of the samples at 525°C to constant weight (AOAC, 923.03).
Total lipids were extracted in Soxhlet apparatus for 6 h using ethyl ether as solvent extractor
(AOAC, 923.05). Total carbohydrates were calculated by difference (100 – (Σ protein + total
lipids + total minerals)).
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26
Photograph 1. Plant images of four Opuntioideae species growing at the Samalayuca area:
(1) O. polyacantha var. arenaria, (2) O. engelmannii, (3) O. macrocentra, and
(4) O. phaeacantha. Fruits and morphological analysis of seeds are shown in
the same column for each species.
Total Phenolics
Phenolic compounds were extracted with 80% (v/v) methanol solution according to the protocol
of Alvarez-Parrilla et al. (2010a). Briefly, 0.1 g of each sample was weighed into screw–cap
tubes. Then 5 mL of the solvent was added, sonicated for 15 min, and centrifuged at 4,000 rpm
for 15 min. This process was performed twice, and the extracts were placed quantitatively in
1 2 3 4
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27
10 mL volumetric flask. One hundred microliters of the above extracts were taken and 500 µL
of the Folin-Ciocalteu reagent was added allowed to stand for 2 min. Thereafter, 400 µL of
Na
2
CO
3
were added and incubated at 50°C for 15 min. Finally, the mixture was cooled in an
ice bath, 250 µL were collected and placed in a microplate well. Absorbance was measured at
740 nm in a BioRad x Mark Plus (Hercules, CA, USA), and the data were obtained with the
Microplate Manager 6.0 (Tokyo, Japan) computer software. A calibration curve was performed
using gallic acid as a standard and the results were expressed as milligrams gallic acid
equivalents (GAE) by 100 g of dry sample.
Determination of Antioxidant Activity by DPPH Method
Antioxidant capacity was analyzed following the method of Alvarez-Parrilla et al. (2010b). The
solutions were made in 80% methanol. DPPH solution (60 mM) was prepared in methanol; 5
µL of the extract were added to 195 µL of the DPPH solution and the absorbance read at 517
nm every min for 1 h. TROLOX was used as standard and results were expressed as mmol
TROLOX equivalents per 100 g dry seed (TE/100 g).
Fatty Acids Profile by Gas Chromatography
The fatty acid profile was determined by gas chromatography in accordance with the procedure
of Núñez-Gastélum et al. (2011). Briefly, 0.5 g dry sample was weighed in a tube with a screw
cap and treated with 2 mL of toluene and 3 mL of HCl methanolic 5% (v/v). The mixtures were
vortexed and placed into a water bath for 2 h. After the samples had cooled to room
temperature, 3 mL K
2
CO
3
6% and 2 mL of toluene was added to the sample, and followed by
agitation in the vortex. The samples were then centrifuged for 5 min at 2,400 rpm (Compact II
Centrifuge, Clay Adams, Sparks, MD). Once the organic phase was separated and dried with
Na
2
SO
4
anhydride, 1 mL of the organic phase was filtered with a 0.45 mm membrane. All
samples were analyzed in triplicate. The equipment consisted of a gas chromatograph 3800
with a flame ionization detector, with a capillary column CP-Sil 88 (60 m x 0.25 mm i.d.,
thickness of 0.25 mm) and a CP-8410 auto-injector, all from Varian Inc. (Palo Alto, CA).
The injection volume was 1 mL (at 220°C), the carrier gas was helium (1 mL min
-1
), and the
detector temperature was held constant at 235°C. The column temperature was held at 120°C
for 1 min, then increased to 170°C at a rate of 3°C min
-1
, held 1 min, and finally augmented to
235°C, which was maintained for 5 min. Peak identifications were based on comparing
retention times with the standards. The area of the peaks was quantified using the software
Galaxie Workstation (Varian Inc., Palo Alto, CA). The relative amount of each fatty acid
(percentage of a fatty acid in total fatty acids) was quantified by integrating the area under the
peak and dividing the result by the total area for all fatty acids.
Statistical analysis
Normality of frequency distributions was tested by the Kolmogorov–Smirnov test. A one–way
ANOVA was performed to test for differences in fruit and seed morphometry data. Pearson’s
correlation was carried out to test for correlation between fruit and seed morphometry.
Statistical analysis was conducted using SPSS v.8.0 software (SPSS Inc. Chicago, IL, USA).
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28
RESULTS AND DISCUSSION
The ecological and economic importance of Opuntioideae species in the Desert of Chihuahua
region, and the practical consequences of large scale surveys with the purpose of such as
identifying source of plantations by the conservation purposes would be enough to justify the
present work. Until now, few studies of Opuntioideae variability based in morphological and
composition of their seeds have been conducted in Samalayuca area. In the present study,
Opuntia natural variability has been assessed by making a comparison of morphological traits
and chemical composition of the seed from different native species. Results revealed
statistically significant differences in seed traits (Table 1). O. polyacanta var. arenaria
presented the highest values in seed weight, seed area, seed length, seed width, embryo plus
cotyledon, and coat areas; however, O. engelmannii had the lowest ones.
Table 1. Seed morphology of four Opuntia species collected from Samalayuca area. The
descriptive statistics are presented in terms of the mean ± SD. Mean values with the
same letters indicate homogeneous subsets for P≤0.05 according to Duncan test.
Morphological
characteristics O. polyacantha O. engelmannii O. phaeacantha O. macrocentra
Seed (g) 0.028 ± 0.00
c
0.009 ± 0.00
a
0.026 ± 0.00
c
0.017 ± 0.00
b
Seed area (mm) 19.69 ± 2.18
c
8.38 ± 1.41
a
14.04 ± 1.60
b
13.15 ± 1.56
b
Seed length (mm) 5.42 ± 0.58
c
3.54 ± 0.32
a
4.55 ± 0.23
b
4.33 ± 0.16
b
Seed width (mm) 4.58 ± 0.44
c
3.07 ± 0.36
a
3.77 ± 0.42
b
3.72 ± 0.19
b
Embryo plus
cotyledon area (mm) 6.83 ± 1.04
c
3.65 ± 0.58
a
4.99 ± 0.47
b
4.84 ± 0.66
b
Coat area (mm) 10.23 ± 1.4
c
4.00 ± 0.84
a
7.56 ± 1.12
b
7.23 ± 1.13
b
Chemical composition
The protein content, total phenolics, and DPPH assay were shown differed significantly among
the species. Protein content measurement varied from 10.45 ± 1.17% (O. phaeacantha) to
14.74 ± 0.62% (O. engelmannii) (Table 2). In comparison with other species of the genus
Opuntia, the protein content was similar that previously reported values (11.8 ± 1.17%) (El et
al., 1998). Regarding the content of total lipids, in this study were obtained values of 3 to 4 fold
compared to those observed for the species O. joconostle and O. matudae (Morales et al.,
2012), and only 1.5 times more than O. ficus-indica (El et al., 1998). The total mineral content
was higher for O. joconostle and O. matudae species (Morales et al., 2012), but 3 times lower
than that reported for O. ficus-indica (El et al., 1998). On the other hand, total carbohydrates
were around 70% of the sample constitution, which are very similar value to that observed for
O. heliabravoana (72.97%), O. joconostle (72.62%), and O. ficus-indica (74.68%) (Prieto-
García et al., 2006).
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JPACD 2018 (20): 23-33
29
Total phenolics
The results of the analysis for total phenolic contents demonstrated that seed of Opuntia
species of Samalayuca area are good source of phenolic compounds, varying from 10.78 ±
1.03 (O. polyacanta var. arenaria) to 12.88 ± 0.42 (O. macrocentra) mg GAEm 100 g
-1
(Table
2). There are few reports on the phenolic content and antioxidant properties in seeds of Opuntia
genus. Morales et al. (2012) found higher values, (in excess of 5-fold) for the content of phenolic
compounds for O. matudae and O. joconostle seeds, compared with the present study. DPPH
assay varied from 2.25 ± 0.09 (O. polyacanta var. arenaria) to 4.29 ± 0.35 (O. phaeacantha)
mmol TE 100 g
-1
. Results expressed as mmol TE 100
-1
g were not found for other Opuntia
genus, but the correlation with the phenolic content in the samples was adequate.
Fatty acids content
Currently, the essential fatty acids are of great interest because it of their potential role
preventing human cardiovascular diseases. Some investigations have shown that Opuntia
seed oil present higher content of linoleic acid compared to other plant oil seed, and these
characteristics confirm the suggestion that Opuntia seed may be an interesting natural source
of edible oil containing high amount of healthy fatty acids. In the present study, linoleic acid
(C18:2n6) was the dominating fatty acid in seed ranging from 66.47 ± 0.85% (O. polyacanta
var. arenaria) to 54.35 ± 2.91% (O. phaeacantha) (Table 2). These values presented a similar
proportion to those registered for different cultivar of O. ficus-indica seeds (Chougui et al.,
2013).
However, other authors have found values in the range of 70 and 80% in seed from O. matudae
and O. joconostle species (Guzman-Maldonado et al., 2010; Morales et al., 2012). Oleic acid
(C18:1n9) varied from 15.47 ± 0.24% (O. polyacanta var. arenaria) to 19.42 ± 1.04% (O.
phaeacantha). The percentages obtained in this study were similar to those presented for O.
ficus-indica species (Chougui et al., 2013). Palmitic acid (C16:0) content varied from 11.01 ±
2.06% (O. engelmannii) to 13.72 ± 1.51% (O. macrocentra). These values were in the range
reported for O. ficus-indica cultivars (Morales et al., 2012), but, higher levels of palmitic acid
content have previously been determined for O. ficus-indica species (Osorio-Esquivel et al.,
2011). These authors concluded that the differences in oil content could be related to the
environmental condition and the state of maturation of the fruit.
Stearic acid (C18:0) content varied from 3.60 ± 0.43% (O. polyacanta var. arenaria) to 5.60 ±
0.47 (O. phaeacantha), values which were within the range of 3.3% to 4.2% reported by others
researchers (Morales et al., 2012). Palmitoleic acid (C16:1n7) content varied from 0.19 ± 0.06%
(O. polyacanta var. arenaria) to 1.34 ± 0.12% (O. phaeacantha). Alpha linolenic acid (C18:3n3)
varied from 0.60 ± 0.05% (O. polyacanta var. arenaria) to 2.42 ± 0.33% (O. phaeacantha).
Arachidonic acid (C20:0) varied from 0.26 ± 0.03% (O. polyacanta var. arenaria) to 0.61 ±
0.11% (O. phaeacantha). And eicosenoic acid (C20:1n9) varied from 0.23 ± 0.01% (O.
engelmannii) to 1.74 ± 0.36% (O. phaeacantha). These percentages of oil content were in the
same proportion as those reported in others works (Ramadan and Mórsel, 2003; Mannoubi et
al., 2009; Guzman-Maldonado et al., 2010; Morales et al., 2012). Nonetheless, the contents of
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30
lipids could depend on degree of ripeness, fruit processing, fruit cultivar and storage conditions
(Osorio-Esquivel et al., 2011).
Table 2. Chemical composition, total phenolic, antioxidant activity and fatty acid profile of seeds
of four Opuntia. The descriptive statistics are presented in terms of the mean ± SD.
Mean values with the same letters indicate homogeneous subsets for P≤0.05
according to Duncan test.
Chemical
composition O. polyacantha O. engelmannii O. phaeacantha O. macrocentra
Water content (%) 4.23 ± 0.38
a
4.79 ± 0.54
a
5.09 ± 0.79
a
4.88 ± 0.69
a
Total minerals (%) 2.55 ± 0.38
a
2.57 ± 0.05
a
2.51 ± 0.07
a
2.71 ± 0.09
a
Protein (%) 11.47 ± 1.40
a
14.75 ± 0.63
b
10.45 ± 1.18
a
11.72 ± 1.23
a
Lipids (%) 9.97 ± 2.38
a
10.45 ± 1.38
a
9.23 ± 2.57
a
9.61 ± 0.163
a
Carbohydrates (%)
*
71.78 67.44 72.72 71.08
Total phenolics
**
10.78 ± 1.03
a
12.55 ± 0.23
b
12.87 ± 0.23
b
12.89 ± 0.43
b
Antioxidant activity
***
2.25 ± 0.09
a
3.41 ± 0.20
b
4.30 ± 0.36
c
3.81 ± 0.56
b
C16:0 12.70 ± 0.57
a
11.01 ± 2.06
a
13.47 ± 0.18
a
13.72 ± 1.51
a
C16:1n7 0.19 ± 0.06
a
0.80 ± 0.25
b
1.34 ± 0.12
c
1.05 ± 0.31
b
C18:0 3.60 ± 0.43
a
3.89 ± 0.45
a
5.60 ± 0.47
b
3.77 ± 0.32
a
C18:1n9 15.47 ± 0.24
a
16.47 ± 0.65
a
19.42 ± 1.04
b
15.70 ± 0.14
a
C18:2n6 66.47 ± 0.85
b
66.27 ± 3.82
b
54.35 ± 2.91
a
63.99 ± 3.03
b
C18:3n3 0.60 ± 0.05
a
0.62 ± 0.49
a
2.42 ± 0.33
b
0.77 ± 0.22
a
C20:0 0.26 ± 0.03
a
0.26 ± 0.03
a
0.61 ± 0.11
b
ND
C20:1n9 0.62 ± 0.06
b
0.23 ± 0.01
a
1.74 ± 0.36
d
0.82 ± 0.08
c
*
Calculated by difference;
**
mg GAE by 100 g sample in dry weight;
***
mmol TE by 100 g dry seed; ND:
No detected
In order to determine if external and internal seed morphological traits, and chemical
composition among the distinct Opuntia species could be related, a Person’s correlation was
made. The results showed that the protein content was inversely correlated with seed weight
(r = −0.672) and seed area (r = −0.578). Notably, total phenolic content was inversely correlated
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JPACD 2018 (20): 23-33
31
(p< 0.01) with seed area (r= −0.671), seed length (r= −0.687). DPPH assay was inversely
correlated with seed weight (r = −0.693).
CONCLUSION
This study discusses for first time the major morphological and nutritional characteristics of
seeds of common Opuntia, collected in Samalayuca area of Chihuahuan Desert. The results
could encourage further application of these seeds of Opuntia as a novel and non-conventional
source of functional food, oils and nutraceuticals, mainly due his abundance. Seed of O.
phaeacantha could be an important new source of health-promoting polyunsaturated fatty acid
and its use in arid and semi-arid regions should be encouraged.
ACKNOWLEDGEMENTS
We would like to thank to the Departamento de Ciencias Químico-Biológicas of the Universidad
Autónoma de Ciudad Juárez for the use of the laboratory and their facilities to obtain the
characterization of Opuntioideae species. Also, we are grateful with technician of USDA MSc.
Irazema Fuentes-Bueno a native english speaker, who has made language corrections.
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