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Heliyon 10 (2024) e34990
Available online 20 July 2024
2405-8440/© 2024 Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/).
Research article
Physicochemical, nutritional properties, and antioxidant potential
of ‘limilla’ fruit (Rhus aromatica var. schmidelioides
(Schltdl.) Engl.)
Gonzalo Soria-Melgarejo
a
,
b
, Juan C. Raya-P´
erez
a
, Juan G. Ramírez-Pimentel
a
,
Jorge Covarrubias-Prieto
a
, Glenda M. Guti´
errez-Benicio
a
,
c
,
Isaac Andrade-Gonz´
alez
d
, Cesar L. Aguirre-Mancilla
a
,
*
a
Tecnol´
ogico Nacional de M´
exico/I.T. de Roque, km 8 Carretera Celaya-Juventino Rosas, C.P. 38110, Celaya, Gto, Mexico
b
Tecnol´
ogico Nacional de M´
exico/I.T.S. de Puru´
andiro, km 4.3 Carretera Puru´
andiro-Galeana, C. P 58532, Puruandiro, Mich, Mexico
c
Universidad de Guanajuato, Programa de Biotecnología, Mutualismo 303, C.P. 38060, Celaya, Gto, Mexico
d
Tecnol´
ogico Nacional de M´
exico/I.T. de Tlajomulco, km 10 Carretera Tlajomulco-San Miguel Cuyutl´
an, Cto. Metropolitano Sur, 45640 Tlajomulco
de Zú˜
niga, Jal, Mexico
ARTICLE INFO
Keywords:
Rhus aromatica
Fragrant sumac
Wild fruit
Bioactive compounds
Polyphenols
Flavonoids
Antioxidants
ABSTRACT
Rhus aromatica inhabits humid oak and oakpine forests in the State of Michoac´
an (Mexico). The
fruit of R. aromatica is edible and is traditionally used in the preparation of soft drinks, ice pops,
ice creams and ‘atole’. The objective of the present investigation was to carry out a physical and
chemical characterization and analysis of the antioxidant capacity of fruit. For the physical
characterization, the equatorial and longitudinal diameter, weight and percentage of pulp were
determined. In the chemical characterization, a proximal analysis was carried out, quantication
of polyphenols and avonoids was performed, and the antioxidant capacity was determined. The
results showed that the fruit had a longitudinal diameter of 6.58 ±1.02 mm, an equatorial
diameter of 7.17 ±0.66, a weight of 55.22 ±5.47 mg, and a 40 % pulp proportion. The chemical
characterization analysis indicated 8.7 % moisture, 30.6 % lipids, 8.7 % proteins, 29.4 % total
sugars, 3.8 % ashes and 18.7 % crude bre, 3.1 ◦Brix, pH 3.1, 1.92 % acidity total and a caloric
intake of 4.27 kcal/g. The polyphenol content was higher in 60 % ethanol extracts with 88.6 ±
50.89 mg EAG/g; for avonoids from extracts with 100 % acetone, it was 26.52 ±0.65 mg EQ/g,
and the total carotenoid content was 46.37 mg/100 g. The total antioxidant activity was higher in
extracts with 80 % acetone, with 87.17 % inhibition of the DPPH radical and 90 % inhibition of
ABTS without showing a signicant difference with the different solvents used. The lowest IC
50
values were presented in 100 % ethanol and 60 % methanol extracts for the DPPH radical and for
the ABTS radical were the 80 % ethanol and 60 % methanol extracts. The lipid, protein, carot-
enoid, and polyphenol contents and antioxidant capacity of the fruit of R. aromatica were as high
as those of other fruits consumed in the human diet.
* Corresponding author.
E-mail address: cesar.am@roque.tecnm.mx (C.L. Aguirre-Mancilla).
Contents lists available at ScienceDirect
Heliyon
journal homepage: www.cell.com/heliyon
https://doi.org/10.1016/j.heliyon.2024.e34990
Received 29 August 2023; Received in revised form 18 July 2024; Accepted 19 July 2024
Heliyon 10 (2024) e34990
2
1. Introduction
The edible fruits of various plant species have considerable levels of functional compounds that provide health benets beyond
their basic nutritional value [1,2]. Among the active compounds that provide functional attributes, natural antioxidants have drawn
attention due to their safety and broad therapeutic effects [3]. The trend to consume little-known wild edible fruits is due to the
numerous benecial health effects and organoleptic properties. Great interest has been shown in wild fruits due to their importance as
a supplement in the diet of rural populations [4–6]. However, the consumption of wild fruits has decreased because conventional fruits
have been improved genetically and agronomically. In this situation, scientic validation of the benecial contributions to health and
nutritional value would increase the added value of wild fruits [7,8]. The rescue of wild species, sustainable development in rural
communities and food security, together with interest in the use of underutilized species, could allow the resumption of the use and
consumption of wild fruits [9–11].
Regarding the bioactive properties of wild fruits, most research has focused on demonstrating their antioxidant properties [7]. The
evaluation of the antioxidant activity in fruits is important since various studies have shown that the intake of some types of fruits has
been related to a lower risk of suffering from cancer and has also been related to the prevention of chronic degenerative diseases
[12–14]. Polyphenols, avonoids and carotenoids are bioactive compounds present in foods of plant origin. The study of these
compounds in foods of natural origin has increased in recent years due to their importance in protecting health and improving
nutrition and their high antioxidant capacity against the action of free radicals; therefore, they contribute to disease prevention [15].
Fruits contain bioactive phenolic compounds such as avonoids, phenolic acids, stilbenes, coumarins, tannins, and anthocyanins,
among others, which play an important role in the attenuation of free radicals [16–18].
Carrying out studies that focus on compounds present in wild fruits with a benecial effect on health may help to understand the
benets and promote a greater consumption of these fruits, including their use for the formulation of functional foods, nutraceutical
and pharmaceutical products, and increase the variety in diet [19].
Rhus aromatica, commonly called fragrant sumac, also known locally as ‘limilla’, ’jaripos’ or ’agrillos’, is a wild fruit produced by a
plant that belongs to one of the 250 species of the Rhus genus. Species in this genus are widely distributed in temperate and tropical
regions around the world. In Mexico, it is possible to nd R. aromatica fruit in the area of ‘El Bajío’, which includes the states of
Michoac´
an, Guanajuato and San Luis Potosí. In the municipality of Puru´
andiro, Michoac´
an state, the fruit is collected by the in-
habitants and is sold during the months of April to June, but its use is limited only to the preparation of soft drinks, ice cream, ice pop
and ‘atole’ [20].
More than 200 chemical components have been identied in fruits of species of the genus Rhus. The main chemical components
include hydrolysable tannins, phenolic acids, anthocyanins, avonoids, organic acids, terpenoids and essential oils in the case of
R. coriaria [21]; antioxidants, phenolics (gallic acid, tannic acid) and avonoids in R. chinensis [22]; and avonoids, anthocyanins and
pyranoanthocyanins in R. typhina [23]. The aforementioned components are attributed to different pharmacological properties, such
as antileishmanial, antibacterial, antioxidant, anti-inammatory, antidiabetic, antihyperlipidemic, neuroprotective, and car-
dioprotective properties, ameliorating hepatic glycolipid metabolism disorder [24–30]. However, for the species R. aromatica, basic
information such as physicochemical characteristics, proximal composition, and the presence of antioxidant components is limited.
Therefore, it is important to explore the chemical composition and biological activity in the fruits of this species.
Some reports have described that fruits of other species of the Rhus genus (R. coriaria, R. chinensis, and R. typhina) have bioactive
properties due to the presence of avonoids, isoavonoids, hydrolysable tannins, anthocyanins, and other phytochemical components,
which are compounds responsible for antimicrobial, anticancer, antihyperglycemic, antihyperlipidemic, anti-inammatory, and
antioxidant activities [21–23]. However, for the species R. aromatica, basic information such as physicochemical characteristics and
proximal composition is limited; therefore, it is important to explore the chemical composition and biological activity of the fruits of
this species. Another type of compound with antioxidant potential and an important role in disease prevention is carotenoids, which
are important lipophilic secondary metabolites with antioxidant properties [31]. There is no report on the presence of this type of
compound in species of the genus Rhus because carotenoids are natural pigments of yellow, orange and red colors, and the presence of
these compounds in the fruits of species of the genus Rhus was assumed. Therefore, the objective of this research was to determine the
physical properties and chemical composition of the R. aromatica fruit, as well as to quantify the total content of phenolic compounds,
avonoids, carotenoids, and antioxidant capacity.
2. Materials and methods
The fruits of R. aromatica were acquired in stores in the municipality of Puru´
andiro (Michoac´
an state, Mexico). The fruits were
selected and allowed to dry for 24 h at 40 ◦C in a drying oven (Novatech, HS45AID, Mexico).
2.1. Determination of physical characteristics of the fruit: weight, dimensions and proportion of pulp-seed
The physical characteristics of the fruit were evaluated from 50 fruits with commercial maturity taken at random, to which the
weight was determined with the help of an analytical balance (Precisa, Switzerland-Dietikon). The longitudinal and equatorial
diameter and thickness of the fruit were measured with a digital Vernier calliper (Luzeren, Mexico). The seed was separated from the
pulp, and the mass of both parts was determined to calculate the proportion of the pulp.
G. Soria-Melgarejo et al.
Heliyon 10 (2024) e34990
3
2.2. Determination of the physicochemical characteristics: ◦Brix, titratable acidity, pH, and soluble solids
To determine degrees Brix (◦Brix), titratable acidity and pH, 2 g of dehydrated pulp was mixed with 100 ml of distilled water [32].
The pH was measured using a potentiometer (HANNA Instruments, Romania). Soluble solids were measured with a portable digital
refractometer (HANNA Instruments, Romania). The titratable acidity was obtained from 100 mL of the aqueous solution of the fruit
mixed with 0.3 mL of 1 % phenolphthalein as an indicator, and the titration was carried out with 0.1 N NaOH. The results were
expressed as % citric acid (% w/w).
2.3. Proximal composition
2.3.1. Determination of moisture content
The moisture content (Hbs) of the fruit was determined by the oven-drying method [33]. Ten grams (mh) of fresh fruit was weighed
to dehydrate in a drying oven (Novatech, HS35-ED, Mexico) at 80 ◦C until a constant weight (ms) was achieved. The moisture per-
centage was calculated using the following formula:
Hbs (%) =(mh-ms)/ms ×100
2.3.2. Determination of total lipid content
The total lipid content determination was carried out using the Soxhlet method [34]. Briey, 3 g of sample (m) was placed in a
cellulose cartridge for extraction, 200 mL of hexane was added to the system, and the extraction was carried out by recirculating the
solvent for 2 h. Then, the solvent was evaporated, and the extract (m2) was obtained. The fat content present in the sample was
calculated with the following formula:
Crude fat (%) =(m2-m1)/m ×100
where m is the weight of the sample; m1 is the weight of the ask alone; and m2 is the weight of the ask with grease.
2.3.3. Determination of ash content
The ash content was determined by the mufe calcination method [35]. Two grams of dry sample was weighed into a clean
porcelain crucible (W1) and placed in a mufe (Novatech, HS35-ED, Mexico) for approximately 5 h at a temperature of 500 ◦C. After 5
h, the crucible was removed and placed in a desiccator until it cooled, and its nal weight (W2) was recorded. The total ash content was
calculated with the following formula:
Ash content (%) =(W2/W1) ×100
2.3.4. Determination of total carbohydrates
The total carbohydrate content was quantied by the phenol-sulfuric method [36]. From an extract prepared with 0.1 g of dried
fruit in 5 ml of distilled water. The reaction was carried out by mixing 125
μ
L of the previously prepared extract with 250
μ
L of 5 %
aqueous phenol and 625
μ
L of concentrated H
2
SO
4
and recording the absorbance at 490 nm. The calculation of total carbohydrates was
carried out using the equation obtained from the calibration curve that was constructed from the known glucose concentrations 0.2,
0.6, 1.0, 1.4, 1.8 and 2.0
μ
g/mL.
2.3.5. Determination of crude protein content
Crude protein was determined according to the micro-Kjeldahl method [37]. Briey, 1.0 g pulverized dry sample was digested in
10 mL H
2
SO
4
at 420 ◦C using copper sulfate and potassium sulfate as the catalyst mixture. The digested sample was distilled using 40 %
NaOH. Ammonia was captured in a 4 % boric acid solution and then titrated with 0.02 N HCl to estimate the total nitrogen content. The
crude protein content was evaluated using a factor of 6.25.
2.3.6. Determination of bre content
The bre content was determined by the AOAC [38] nonenzymatic gravimetric method with some modications. Defatted and
pulverized 2 g samples were boiled in 0.25 N H
2
SO
4
solution for 30 min. Next, the hydrolysed fraction was ltered using a Buchner
funnel, and the residue was washed with water. The residue obtained was boiled in a 0.3 N NaOH solution for 30 min, ltered under
vacuum and washed with hot water. The residue obtained was washed with a 0.25 N H
2
SO
4
solution and then with hot water, followed
by three washes with petroleum ether. The nal residue was placed in a crucible and dried in an oven at 105 ◦C for 12 h. After the
drying time, the mass of the crucible with residue was recorded, and then it was introduced into a mufe furnace at 550 ◦C for 3 h.
Then, it was cooled, and the mass of the nal residue was recorded to carry out the corresponding calculation with the following
equation:
Fibre content (%) =(A-B)/C ×100
G. Soria-Melgarejo et al.
Heliyon 10 (2024) e34990
4
where A is the weight of the crucible with dry residue (g), B is the weight of the crucible with ash (g), and C is the weight of the sample
(g).
2.3.7. Caloric intake
The caloric intake of the fruit was calculated using the Atwater factors: 9 kJ/g lipids, 4 kJ/g carbohydrates and 4 kJ/g proteins [39].
2.4. Preparation of extracts
The fruit pulp, separated from the seed, was dehydrated at 40 ◦C in a convective dryer for 24 h. For this study, extracts were
prepared in glass bottles from 0.125 g of pulp with 5 ml of the different solvents under agitation for 24 h at room temperature (25 ◦C) in
the dark; the solvents used were absolute methanol, 80 % methanol, 60 % methanol, absolute ethanol, 80 % ethanol, 60 % ethanol,
absolute acetone, 80 % acetone and 60 % acetone. The extracts were centrifuged at 1500 rpm to obtain the supernatant, and the
quantication of polyphenols, avonoids and antioxidant capacity was immediately performed [40,41].
2.4.1. Quantication of total polyphenols and avonoids
The total content of polyphenols was determined by the Folin-Ciocalteu method [42] with some modications; the calibration
curve was made with gallic acid at concentrations of 40, 80, 120, 160, 200, 240, 280, 320, 360, 380, 420 and 500
μ
g/mL. Fifty mi-
croliters of each concentration was taken, 750
μ
L of distilled water and 50
μ
L of Folin-Ciocalteu reagent were added, and the mixture
was left to settle for 3 min. Then, 150
μ
L of 15 % sodium carbonate solution was added, and the mixture was incubated for 30 min at
50 ◦C. After incubation, 250
μ
L of each of the prepared solutions was used to measure the absorbance in a microplate absorbance
spectrophotometer (Bio-Rad, xMarkTM, USA) at a wavelength of 760 nm. For the quantication of total polyphenols in the extracts, 50
μ
L of the extracts was used. The calculation of total polyphenols was carried out using the equation obtained from the calibration
curve, and the result was expressed in equivalent milligrams of gallic acid/g of dry weight (mg EGA/g).
The determination of total avonoids was carried out by the formation of aluminum complexes [43]. Fifty microliters of extract was
added to a tube containing 100
μ
L of 1 M potassium acetate, 100
μ
L of 10 % aluminum nitrate and 500
μ
L of 80 % ethanol, and the
mixture was left to rest for 30 min at room temperature. Subsequently, 250
μ
L of the mixture was taken and placed in a microplate, and
the absorbance was read in a spectrophotometer at a wavelength of 415 nm. The calculation of total avonoids in the extracts was
carried out using the equation obtained from the quercetin calibration curve that was built from the concentrations of 60, 100, 140,
180, 220, 240, 280 and 300
μ
g/mL, and the results were expressed in milligrams quercetin equivalents/g dry weight (mg EQ/g).
2.4.2. Determination of total carotenoid content
The determination of carotenoids was performed by spectrophotometry, with some modications [44]. Briey, 2 g of dried fruit
was homogenized in 20 mL of a mixture of acetone:ethanol (1:1) and left to settle for 24 h at 4 ◦C. Subsequently, the solution was
ltered and adjusted to 100 mL with an acetone:ethanol (1:1) mixture. Then, the solution was transferred to a separatory funnel, 50 mL
of hexane and 25 mL of water were added, and the mixture was stirred for 5 min. The mixture obtained was left to rest for 30 min for
phase separation. The organic phase was recovered, and the absorbance was measured at 470 nm in a microplate spectrophotometer
(Bio-Rad, xMark ™, USA). The results were expressed as
μ
g β-carotene equivalent/100 g using the following equation:
μ
g β carotene equivalent/100 g =(A ×V ×106) /A1cm ×100 ×PMx
where A is the sample absorbance, V is the total volume of the extract (mL), A1cm is the β-carotene absorptivity coefcient (2500), and
PMx is the sample weight (g).
2.5. Antioxidant capacity
Because antioxidant capacity is a complex property, it is recommended to use more than one method to measure it. For this study,
the ABTS and DPPH assays were chosen. The rst allows the determination of the antioxidant capacity of both lipophilic and hy-
drophilic compounds, which is an advantage due to the type of solvents used for the preparation of the extracts. The DPPH assay
evaluates the antioxidant capacity of hydrophilic compounds that have been extracted with organic solvents in solution.
2.5.1. Antioxidant capacity, DPPH assay
The antioxidant capacity of pulp extracts from R. aromatica fruits was evaluated using the DPPH assay [45] with some modi-
cations [46]. The 0.1 mM DPPH radical was adjusted to an absorbance of 0.75 at a wavelength of 515 nm using a spectrophotometer.
Next, 230
μ
L of the radical with 20
μ
L of extract was placed in a microplate, the mixture was incubated in the dark at room temperature
for 30 min, and the absorbance at 515 nm was measured and contrasted against control samples. Antioxidant activity was expressed as
the percentage of DPPH radical scavenging activity (% RSA) relative to the control. The dose response was also obtained at different
concentrations of methanolic extracts against the radical (0.1, 0.5, 1.0, 2.0, 4.0 and 6
μ
g/ml). Finally, the effective concentration of
antioxidant required to decrease the initial concentration by 50 % (IC
50
) was determined according to Brand-Williams et al. [47].
2.5.2. Antioxidant capacity, ABTS assay
The antioxidant capacity assay by ABTS (2,2
′
-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid)) was performed as described by Re
G. Soria-Melgarejo et al.
Heliyon 10 (2024) e34990
5
et al. [48] with some modications. The stock solution was prepared with 14 mM ABTS mixed with 2.6 mM potassium persulfate and
left to rest for 24 h at 4 ◦C. To carry out the assay, the solution was adjusted to an optical density of 0.75 at 734 nm. A total of 230
μ
L
was placed in a microplate of the ABTS radical and 20
μ
L of the extracts at the concentrations already described for the DPPH assay,
and the absorbance was read. In both DPPH and ABTS assays, the decrease in absorbance of the sample indicates the capacity to
eliminate free radicals. For this test, the dose response of the extracts and the IC
50
value were also determined.
2.6. Statistical analysis
The experimental design was completely random with three replications. The analysis was performed using Statistix software ver
10 (Analytical Software 2105 Miller Landing Rd Tallahassee, FL 32312, USA); mean comparisons were performed by Tukey’s test (p ≤
0.05) when ANOVA showed signicant differences among treatments.
3. Results
3.1. Physical characteristics of the R. aromatica fruit
The fruits of R. aromatica weighed an average of 55.22 ±5.47 mg; the polar and equatorial diameters were 6.60 ±1.02 mm and
7.15 ±0.66 mm, respectively. The dimensions of the fruit allowed us to characterize it as a subglobular fruit, and these data allow the
design of processes for the selection, cleaning and classication of the fruit. On the other hand, the portion of the pulp (edible)
represented 40 % in relation to the total weight of the fruit, which indicates that it is possible to make an integral use including the
seed.
3.2. Physicochemical characteristics and proximal analysis of the fruit pulp
The results of proximal composition are presented in Table 1; from this analysis, the high content of total fats stands out, so it is
pertinent in future research to carry out a specic characterization of the lipid content of the fruit of R. aromatica.
The values represent the mean of three replications.
Table 2 shows the percentage of the requirement pattern of the proximal components [49–51] and the percentage of contribution of
the ‘limilla’ per 100 g of fruit. The results of this work show that ‘limilla’ fruit is a good source of lipids and is low in carbohydrates.
3.3. Content of polyphenols, avonoids and carotenoids
Polyphenolic compounds are important since they are nonnutritive components synthesized by the secondary metabolism of plants
and play an important role in human health, in addition to presenting various bioactive properties [52,53]. The content of total
polyphenols quantied in the pulp of the R. aromatica fruit presented signicant differences (p ≤0.001) depending on the solvent and
the proportion of water used to obtain the extracts (Fig. 1). The content of total polyphenols was higher in the extract obtained with 80
% methanol, followed by the extracts obtained with 60 % ethanol and 60 % acetone (Table 3). With these results, it is conrmed that
polar organic solvents mixed with water allow the extraction of phenolic compounds more efciently, possibly due to the presence of
glycosides with external hydrophilic hydroxyls in the chemical structure [54,55].
Flavonoids are the most common type of polyphenols and are mainly divided into six classes based on the degree of oxidation.
These classes include avones, isoavones, avanones, avonols, anthocyanins, and proanthocyanidins [56]. The quantication of the
total avonoid content yielded signicant differences (p ≤0.001) depending on the solvent and the proportion of water used to obtain
the extracts. The majority of total avonoids were obtained in the extracts with acetone, ethanol, and methanol, all at 100 %; the
highest amount of polyphenols was obtained with 100 % acetone (Table 3).
Carotenoids are natural compounds responsible for the typical colors of some fruits that give them red, orange and yellow tones,
depending on their type and content; in this regard, ‘limilla’ fruit is typically associated with shades of red‒orange color. Table 4 shows
the content of total carotenoids expressed in mg β-carotene equivalents/100 g of fruit and the contribution with respect to other
Table 1
Proximal composition of R. aromatica fruits.
Component Rhus aromatica
Moisture (%) 8.7
Ash (%) 3.8
Fat (%) 30.6
Crude Protein (%) 8.7
Crude Fibre (%) 18.7
Total Carbohydrates (%) 29.4
Caloric Intake (kcal/100 g) 415.8
pH 3.1
◦Brix 3.1
Titratable acidity 1.9
G. Soria-Melgarejo et al.
Heliyon 10 (2024) e34990
6
sources of fruits and vegetables of daily consumption reported by other authors [57–59].
3.4. Antioxidant capacity
The total antioxidant capacity was signicantly (p ≤0.001) different depending on the solvent used for the extraction (Fig. 1). The
highest values of total antioxidant activity (80–87.17 %) were obtained in extracts with 80 % methanol, 80 % ethanol and 80 %
acetone.
Table 2
Proximate composition of R. aromatica and percentage contribution with respect to the requirement patterns for different age groups.
Component Infants Children Adults
0.5–1 year 1–3 years 4–8 years 9–13 years 14–18 years >18 years
Contribution of R. aromatica (g/100 g) RP RCP RP RCP RP RCP RP RCP RP RCP RP RCP
Carbohydrates 29.4 60–95 49–31 130 23 130 23 130 23 130 23 130 23
Fat 30.6 30 100 22 133 22 133 63 133 22 133 22 133
Protein 8.7 9–13 96–64 13 70 19 46 34 26 52 17 56 16
Fibre 18.7 ND ND 19 98 25 75 31 60 38 49 38 49
RP =Requirement patterns for the different age groups (grams of component). %RPC=Contribution to the percentage requirement. ND=Not
determined.
Fig. 1. Free radical scavenging activity of DPPH from R. aromatica extracts (mean ±SD, n =3). Bars with the same letter are not signicantly
different (Tukey’s test, p ≤0.05).
Table 3
Total content of polyphenols and avonoids in the pulp of R. aromatica fruits.
Solvent Total polyphenols (mg AG/g) Total avonoids (mg EQ/g)
100 % MeOH 66.53 ±0.45 f 17.45 ±0.33 c
80 % MeOH 80.55 ±0.62 c 7.30 ±0.18 g
60 % MeOH 71.71 ±1.13 e 10.09 ±0.21 e
100 % EtOH 62.28 ±0.13 g 19.29 ±0.69 b
80 % EtOH 72.50 ±0.90 de 8.38 ±0.47 fg
60 % EtOH 88.65 ±0.89 a 9.22 ±0.15 ef
100 % Acetone 56.98 ±0.19 h 26.52 ±0.65 a
80 % Acetone 74.28 ±0.15 d 10.35 ±0.58 e
60 % Acetone 85.94 ±0.05 b 12.78 ±0.13 d
Values in the same column with a different letter are signicantly different (Tukey, p <0.05). The values shown represent
the mean ±standard deviation.
Table 4
Total content of carotenoids in R. aromatica and other fruits consumed daily.
Source mg total carotenoids/100 g of fruit Contribution with respect to R. aromatica (%)
R. aromatica 46.37 ±3.27
a
100
Mango 7.47 [57] 16
Orange bell pepper 6.99 [58] 15
Carrot 5.47 [59] 11.7
Mammy 4.42 [59] 9.5
a
The data is the mean value with standard deviation, n =3.
G. Soria-Melgarejo et al.
Heliyon 10 (2024) e34990
7
In the ABTS assay (Fig. 2), the extracts with different solvents and proportions of water did not show a signicant difference in the
total antioxidant capacity, and the radical elimination capacity in the different extracts was 90 %. A similar effectiveness was
determined in fruits of R. chinensis Mill [60].
In Figs. 3–5, the antioxidant capacity in dose response is shown; most of the extracts presented a DPPH free radical scavenging
capacity greater than 60 % at concentrations of 4
μ
g/mL, except for the extracts with pure acetone and 80 % acetone. The best values of
radical elimination capacity (greater than 80 %) were obtained with 6
μ
g/mL from the different 80 % and 60 % solvents, which allows
an advantage for the use of more environmentally friendly solvents to obtain compounds with antioxidant capacity.
On the other hand, IC
50
was also determined with DPPH and ABTS; in both trials, the values obtained were signicantly different
between the different extracts tested (p <0.05). The lower the IC
50
value, the better its radical inhibition capacity. The IC
50
values
obtained according to the solvents used at the different concentrations are shown in Table 5.
The best IC
50
values for the inhibition of DPPH radicals were obtained with the extracts with 60 % methanol and 100 % ethanol,
although they were not signicantly different from the IC
50
value obtained with 80 % MeOH. For ABTS, the best IC
50
values were
obtained with 80 % EtOH, 60 % MeOH, 80 % acetone, and 80 % MeOH.
4. Discussion
R. aromatica has physical characteristics similar to fruits of other species of the same genus (Rhus) and are described as subglobular
fruits. Such is the case for the fruit of R. coriaria, which has a thickness of 2.51 mm and polar and equatorial diameters of 4.98 mm and
5.54 mm, respectively [61]. Similar to the percentage of pulp found for the fruit of R. aromatica below 50 %, it has been reported for
other species of the genus Rhus that the majority percentage is seed, such as Rhus chinensis, where the seed represents 78 % of the fruit
[62]. The value of total soluble solids of R. aromatica is similar to that reported in R. coriaria [63], so both species lack the possibility of
obtaining juice from their fruits. The pH values (2.66–3.90) reported for R. coriaria fruits [64] are similar to the pH found in this study
for R. aromatica (Table 1); the variation between the pH values even when they belong to the same species can be inuenced by the
amount of organic acids contained in the fruit [65]. The fruits of R. aromatica and R. coriaria are considered to be highly acidic, ac-
cording to the classication of foods with pH values similar to those reported in this study.
The titratable acidity value (2.1–7.8 %) reported for R. coriaria [64] is similar to that of R. aromatica (Table 1). Various in-
vestigations have revealed that the acidic taste of R. coriaria is due to the presence of malic acid; therefore, it could be that malic acid is
the major organic acid of R. aromatica.
The moisture value of R. aromatica (Table 1) was lower than that reported for R. coriaria (9.6 %) [61] and higher than that reported
for R. typhina (6.64 %) [23]. The difference between the moisture values of these fruits may be inuenced by the time the fruit is
collected, since once ripe, depending on the climatic conditions, the fruits tend to lose moisture.
The crude protein content of R. aromatica (Table 1) was higher than that reported for R. coriaria (2.6 %) [61] and for R. typhina
(4.31 %) [23]. In another investigation in R. coriaria [66] and R. chinensis [62], crude protein values of 11.56 % and 9.14–10.55 %,
respectively, were obtained. Regarding the quality of the protein, only the presence of essential amino acids in low amounts has been
reported for R. typhina [23], and for R. coriaria, only the total amount of free amino acids ranges from 25.01 to 166.38 mg GlyE/g DW
[64].
As part of the chemical composition of the fruits that belong to the genus Rhus, the lipid content is the most representative. There is
precedent for interest in the fruits of this genus as an alternative to oilseeds. In this regard, the total lipid content (30.6 %) of
R. aromatica can be considered high compared to that reported for R. coriaria (7.4 %) [61] and R. typhina (11.52 %) [23], so the fruit
could be an adequate source of vegetable lipids, particularly an appropriate source of lipophilic pigments given the waxy consistency
and colouration of the fruit.
Regarding the total bre content, R. aromatica fruit showed a higher content than R. coriaria (14.6 %) [61] and less than R. typhina
(32.9 %) [23]. In this regard, it is known that fruits that present values greater than or equal to 14.6 % of crude bre are a potential
source of dietary bre that could be used to favour gastrointestinal disorders.
The fruit of R. aromatica adequately contributes to the recommended daily intake requirements for all age groups; a high
Fig. 2. Free radical scavenging activity of ABTS from R. aromatica extracts (mean ±SD, n =3). Bars with the same letter are not signicantly
different (Tukey’s test p ≤0.05).
G. Soria-Melgarejo et al.
Heliyon 10 (2024) e34990
8
contribution of bre, carbohydrates and proteins can be highlighted.
Phenolic compounds, also called polyphenols, are metabolic products widely distributed in plant foods; they have biological and
pharmacological activities that could provide protection against chronic diseases [24]. These compounds have a greater antioxidant
effect than vitamins and are capable of neutralizing the effects of oxidative free radicals [40]. There are various investigations in which
the amount of polyphenols and avonoids in fruits of species belonging to the Rhus genus, mainly R. coriaria, R. typhina, and R.
Fig. 3. Dose‒response relationship in the elimination of DPPH radicals from extracts with methanol of R. aromatica fruits. Values are shown as the
mean ±SD (n =3). Means with different letters at the same concentration are signicantly different (Tukey’s test, p <0.05).
Fig. 4. Dose‒response relationship in the elimination of DPPH radicals from extracts with ethanol of R. aromatica fruits. Values are shown as the
mean ±SD (n =3). Means with different letters at the same concentration are signicantly different (Tukey’s test, p <0.05).
Fig. 5. Dose‒response relationship in the elimination of DPPH radicals from extracts with acetone of R. aromatica fruits. Values are shown as the
mean ±SD (n =3). Means with different letters at the same concentration are signicantly different (Tukey’s test, p <0.05).
G. Soria-Melgarejo et al.
Heliyon 10 (2024) e34990
9
tripartite, among others, has been quantied. However, for the species R. aromatica, this study is the rst to quantify these components.
R. aromatica showed a higher content of polyphenols compared to R. coriaria [67], which is reported from 36.38 to 58.66 mg GAE/g in
15 genotypes from extracts with methanol, and other values reported in this range from different populations of R. coriaria where it is
mentioned that the polyphenol content in fruit extracts with 80 % methanol is 77.54 mg GAE/g [74]. On the other hand, concen-
trations similar to those of R. aromatica were found in extracts of fruits with 80 % methanol of the species R. hirta with a content of 81.6
mg GAE/g [68], and values close to those reported in R. tripartite with a content of 102.06 mg GAE/g [69], also in fruit extracts with
methanol. Finally, for R. typhina fruits, the polyphenol content exceeds that reported in this study, with values of 151 mg GAE/g in
extracts with 20 % ethanol [66], and concentrations similar to those reported in extracts of R. hirta with ethanol acidied with 1 % HCl
(81.6 mg GAE/g) [68]. In relation to the solvents for the extraction of total polyphenols, the present investigation coincides with that
reported by Zhang [60], where the highest content of polyphenols was obtained from extracts with 80 % ethanol. Due to the high
content of total polyphenols found in this study for R. aromatica, this fruit can be considered an adequate source of polyphenols since it
exceeds the value reported for fruits of regular consumption: blueberries 7.07 mg/g [70], blackberries 4.12 mg/g [71], strawberries
2.35 mg/g and raspberries 3.09 mg/g [72].
The avonoid content of R. aromatica compared to other species of the same genus is higher; in extracts with 80 % methanol,
R. coriaria fruits presented values between 2.19 and 7.54 mg GAE/g [64]. On the other hand, Wu et al. [68] reported 4.97 mg GAE/g in
extracts with 80 % ethanol, and another author reported 14.28 mg EAG/g in extracts with methanol in fruits of R. tripartita and 11.93
mg EAG/g in R. pentaphylla [69].
Carotenoid content is not reported for species other than R. aromatica (within the Rhus genus). The study of the concentration of
total carotenoids present in ‘limilla’ fruit is relevant since carotenoids are an important part of the human diet. Carotenoids play a vital
role in health and nutrition with positive effects in preventing vitamin A deciency, as well as reducing the incidence of age-related eye
diseases, cancer, and cardiovascular diseases [73]. In addition, there are carotenoids that are used as pigments, such as astaxanthin,
which is added to sh feed to obtain a desirable pink meat color [74]. The ‘limilla’ fruit has a higher content of carotenoids than other
fruits and vegetables of daily use. This rst report on the content of carotenoids in species of the genus Rhus opens the possibility for
future research that elucidates the prole of carotenoids and the biological properties that they can contribute.
The antioxidant capacity of R. aromatica is higher than that reported in fruits of various cultivars of R. coriaria [64,65], of which the
total antioxidant capacity is reported to range from 73.37 to 79 % in extracts with methanol.
The dose‒response obtained for the elimination of DPPH radicals by the fruit extracts of R. aromatica is better than those obtained
from extracts of R. chinensis [60], in which, at a dose of 5
μ
g/mL of extract, the ability to eliminate free radicals does not exceed 70 %.
The dose response for the elimination of ABTS radicals was also more efcient for the extract of R. aromatica because with 4
μ
g/mL of
extract, elimination capacities greater than 85 % and 90 % were obtained in extracts obtained with methanol and ethanol, respectively,
at 100 %. Likewise, a dose‒response is reported for the elimination of ABTS radicals by extracts of R. chinensis at 40 % with a con-
centration of 2.5
μ
g/mL of extract [60], in comparison with a similar concentration of extract (2
μ
g/mL) of R. aromatica, which
eliminates the ABTS radicals in a higher percentage (greater than 60 %), with the exception of the extract with 100 % acetone.
The IC
50
values, with DPPH, obtained with extracts of R. aromatica fruits were lower than those reported in extracts of fruits of other
species of the Rhus genus. For extracts of R. coriaria with ethanol and water, IC
50
values of 20 ±2.6 and 54 ±2.77 were obtained,
respectively [21]. In extracts of R. chinensis with 80 % methanol, 80 % ethanol and 80 % ketone, IC
50
values of 3.72, 3.92 and 3.64 were
obtained, respectively [60]. In the case of extracts with methanol from fruits of R. tripartita and R. pentaphyla, IC
50
values of
22.83–35.47 and 12.90 to 15.09 are reported, respectively [69]. For the ABTS radical, the extracts of R. tripartitum obtained with
methanol showed IC50 values of 3.81–55.5 [75]; compared to the values of this study, they are on the order of two to forty times
higher.
According to the results obtained in this investigation, the content of polyphenols, avonoids and antioxidant capacity, it is
pertinent to investigate further in the identication of specic components of the fruit of R. aromatica and start with the rst studies
that focus on exploring the pharmacological properties of this species.
Table 5
IC
50
values (
μ
g/mL) for the inhibition of DPPH and ABTS radicals from different extracts of R. aromatica fruit.
Extract IC
50
DPPH Extract IC
50
ABTS
100 % EtOH 1.87 ±0.04
d
80 % EtOH 1.32 ±0.04
d
60 % MeOH 1.89 ±0.03
d
60 % MeOH 1.48 ±0.19
cd
80 % MeOH 2.08 ±0.04
cd
80 % Acetone 1.53 ±0.16
cd
80 % Acetone 2.35 ±0.04
bc
80 % MeOH 1.81 ±1.97
bcd
80 % EtOH 2.63 ±0.17
b
100 % EtOH 2.083 ±0.15
bc
60 % Acetone 2.73 ±0.03
b
100 % Acetone 2.25 ±0.10
b
100 % MeOH 3.41 ±0.08
a
100 % MeOH 2.43 ±0.42
b
60 % EtOH 3.54 ±0.20
a
60 % EtOH 2.44 ±0.06
b
100 % Acetone 3.67 ±0.08
a
60 % Acetone 3.23 ±0.10
a
Values are the mean of triplicate determinations (n =3) ±standard deviation; means with different letters are signicantly different
(Tukey p <0.05).
G. Soria-Melgarejo et al.
Heliyon 10 (2024) e34990
10
5. Conclusion
According to the values obtained in this research, the fruit of Rhus aromatica has some similarities to the fruits of species belonging
to the same genus, such as physical characteristics, yield in the edible part, pH, and protein and bre content. However, the lipid
content for the fruit of R. aromatica is higher than that for the other species. On the other hand, due to the values of the total polyphenol
content obtained, the fruit of R. aromatica can be considered an adequate source of polyphenols since it mostly exceeds the values of
other species. Additionally, the results of the antioxidant capacity are higher compared to the other species, so the fruits of R. aromatica
can be considered in future research for the assessment of pharmacological properties focused on antiobesity, anticancer, antimi-
crobial, and antihyperlipidemic effects, among others properties. For the rst time, the content of total carotenoids in the fruit of one of
the species of the genus Rhus (R. aromatica) is reported, presenting a higher contribution than some fruits and vegetables of daily
consumption.
Data availability statement
Data will be made available on request.
CRediT authorship contribution statement
Gonzalo Soria-Melgarejo: Writing – original draft, Methodology, Investigation, Formal analysis, Conceptualization. Juan C.
Raya-P´
erez: Validation, Data curation. Juan G. Ramírez-Pimentel: Visualization. Jorge Covarrubias-Prieto: Validation. Glenda M.
Guti´
errez-Benicio: Validation, Resources. Isaac Andrade-Gonz´
alez: Data curation. Cesar L. Aguirre-Mancilla: Writing – review &
editing, Software, Project administration, Methodology, Investigation, Conceptualization.
Declaration of competing interest
The authors declare that they have no known competing nancial interests or personal relationships that could have appeared to
inuence the work reported in this paper.
Acknowledgements
Thanks to the Consejo Nacional de Humanidades, Ciencia y Tecnología (CONAHCyT, Mexico) for a scholarship awarded to G.S-M.
for postgraduate studies in Agrifood Production Sciences at the TecNM-Instituto Tecnol´
ogico de Roque.
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