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Phenolic acids from fruits of Physalis angulata L. in two stages of maturation

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DOI: 10.1016/j.sajb.2020.02.029

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 South African Journal of Botany 131 (2020) 448 453

Contents lists available at ScienceDirect

South African Journal of Botany

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

Phenolic acids from fruits of Physalis angulata L. in two stages of

maturation
Ana Mery de Oliveiraa, Lovemore N. Malungab, Camila A. Perusselloc,*, Trust Betad,
Rosemary Hoffmann Ribanie
a


Federal Institute of Education, Science and Technology, Department of Fishery Engineering, Piuma, ES, 29285-000, Brazil
b
Richardson Centre for Functional Foods and Nutraceuticals, Smartpark, University of Manitoba, Winnipeg, R3T 6C5, Canada
c
Technological University Dublin, Environmental Sustainability and Health Institute, Grangegorman, D7 H6K8, Dublin, Ireland
d
Department of Food Science, University of Manitoba, Winnipeg, R3T2N2, Canada

e
Graduate Program in Food Engineering, Department of Chemical Engineering, Federal University of Parana
, 81531-980, Curitiba, PR, Brazil

A R T I C L E I N F O A B S T R A C T

Article History: Physalis angulata L. is an exotic fruit of the Solanaceae family, native to the Amazon region, which has been
Received 19 September 2019 widely introduced across many tropical and subtropical regions (e.g. Central and South America, Africa, India
Revised 16 December 2019 and Pacific islands). Often characterized as a pantropical invasive weed of crops, gardens and plantations, it
Accepted 16 February 2020
contains several chemical compounds of biological interest, such as phenolic acids and flavonoids. The pro-
Available online 8 May 2020
files of soluble and insoluble phenolic acids, total phenolic content (TPC) and antioxidant activity of fruits of
Physalis angulata were determined in two stages of maturation in order to expand its consumption. The pre-
Keywords:
dominant phenolic acids in ripe and green fruits were ferulic acid and p-hydroxybenzoic acid. During matu-
Antioxidant capacity
Native fruit
ration, the TPC increased by 9.8%, resulting in a 10.15% higher antioxidant capacity compared to the green
Phenolic acid fruits. The ripe fruits exhibited values of TPC and antioxidant activity higher than those found in ripe Physalis
Ripening peruviana, another fruit of the Solanaceae family, which is already consolidated as a highly functional fruit.
Physalis angulata L. © 2021 The Authors. Published by Elsevier B.V. on behalf of SAAB. This is an open access article under the CC
BY license (http://creativecommons.org/licenses/by/4.0/)

1. Introduction
(Rufino et al., 2010; da Silva et al., 2014; Dutra et al., 2017). Phenolic
compounds found in fruits possess strong antioxidant activity, which
Physalis sp. is a native Amazonian fruit, belonging to the Solana-
is associated with protection against oxidative stress in the body.
ceae family, which occurs in subtropical temperate and warm
These compounds are present in high quantities in exotic and native
weather regions, such as Central and South America, Africa, India and
fruit species largely produced in tropical countries, thereby increasing
Pacific islands. The plant is herbaceous, annual or perennial, and the
the interest of the food industry in these fruits (Dutra et al., 2017).
genus comprises approximately 120 species (Zhang and Tong, 2016).
Several biological activities have been demonstrated to extracts and
The species commonly found are Physalis angulata L. (P. angulata),
bioactive compounds obtained from the stem, roots and aerial parts of
native to Brazil and spontaneously growing in all country, and Physa-
the Physalis angulata L. plant. They have already been described as
lis peruviana (P. peruviana), commercially cultivated in the South of
exhibiting immunomodulatory activity (Soares et al., 2003), immunos-
Brazil, in the Rio Grande do Sul State (Rufato et al., 2008; Leite et al.,
timulant activity (Siley et al., 2017), antitumor activity (Wu et al., 2006;
2018). Physalis sp. has aroused the interest of consumers due to the
Hsieh et al., 2006), anti-inflammatory activity (Choi and Hwang, 2003;
long list of chemical constituents of nutritional and pharmacological
Rivieira et al., 2019), anti-malarial activity (Lusakibanza et al., 2010),
interest, such as phenolic acids or flavonoids, glycosides (kaempferol,
anti-metastasis activity (Hseu et al., 2011) and anti-microbial activity
quercetin, rutin), ascorbic acid, carotenoids, alkaloids and steroids
(Pietro et al., 2000), including antileishmanial activity (Nogueira et al.,
(Silva and Agra, 2005; Silva et al., 2016; Moreira and Dias, 2018).
2013; Silva et al., 2018). The phenolic acids present in the soluble and
Although P. peruviana is consolidated for decades in the South Ameri-
insoluble extracts identified in many fruits correlate with their antioxi-
can fruit market as a high source of biocompounds (Puentes et al.,
dant activity. The variations in the content of these compounds found
2011), little is known about the P. angulata species.
in various fruits and vegetables may be attributed to their complexity
The consumption of tropical fruits has increased in recent
and to the methods of extraction or quantification applied (Balasun-
years due to their popularity as sources of bioactive compounds
dram et al., 2006; Yao et al., 2004).
The fruit of P. angulata (Fig. 1-A) exhibits high ecological adapta-
* Corresponding author.
tion and hence great potential for commercial cultivation in tropical
E-mail address: cami.perussello@gmail.com (C.A. Perussello).

https://doi.org/10.1016/j.sajb.2020.02.029
0254-6299/© 2021 The Authors. Published by Elsevier B.V. on behalf of SAAB. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/)
 A.M. de Oliveira et al. / South African Journal of Botany 131 (2020) 448 453 449

Fig. 1. Physalis angulata L. (A = fruit; B = fruit internal view; C = flower; D = cup)Source: the authors.

and subtropical climates (e.g. Brazil and South Africa). It is classified antioxidant capacity and chemical composition seedless pulp
as a tolerant species due to its adaptation to different soil types and extracts from Physalis angulata L. obtained by pressurized ethanol.
temperate climates. Popularly known in Brazil as camapu
and in The aim of the present study was to characterize the antioxidant
South Africa as cutleaf groundcherry, P. angulata is a climacteric fruit potential of P. angulata at two stages of maturation. Ripe fruits of P.
covered by a calyx (Fig. 1-D), which protects it from adverse environ- peruviana were also assessed for comparison purposes.
mental conditions, and exhibits yellow flowers (Fig. 1-C). When ripe
the fruit has diameter between 1.0 and 1.5 cm and contains 100 to
2. Materials and methods
300 small seeds (Fig. 1-B). The plant is considered a weed of vacant
and crop lands because it grows wildly in the form of small popula-
2.1. Plant material
tions (Lorenzi and Matos, 2008).
The current literature does not report any information on the
P. angulata fruits were planted and harvested at the Experimental
phenolic composition of P. angulata fruits and the behavior of these
Station of the Federal University of Parana
, located in Quatro Barras,
bioactives during maturation. While there are many studies
Metropolitan Region of Curitiba, Brazil. The fruits were harvested
reporting the pharmacological effects of the genus Physalis as a
80 days after planting and were visually classified into two maturity
result of the high quantities of withanolides and physalins found
stages according to their color intensity: green, when the epicarp was
in the whole plant or its parts (Chang et al., 2016; Sisley et al.,
totally green, and ripe, when it was totally yellow-purple or yellow.
2017; Leite et al., 2018; Anh et al., 2018; Rivieira et al., 2019), few
The visual scale employed was based on the scale proposed by Fischer
are related to the fruit’s antioxidant activity and phenolic profiling.
et al. (2005). Color of the peel is considered as the first quality parame-
Furthermore, most investigations were carried out on Physalis
ter evaluated by consumers and it is associated with specific tastes or
peruviana, which is a different species with accordingly different
uses that can determine their acceptance or rejection. According to
chemical composition and antioxidant properties (Zamora-Tavares
Mendoza and Aguilera (2004), peel color correlates well with physical
et al., 2016). The literature focuses on the influence of extraction
and chemical changes that take place during ripening. The ripe fruits
conditions in obtaining these compounds, especially from the
of P. peruviana, used as a comparison sample, were purchased in the
whole plant. Kusumaningtyas et al. (2015) determined the total
CEASA Market of Curitiba (Brazil). The fruits were frozen ( 18 °C),
phenolic content and antioxidant activity in Physalis angulata L.
freeze-dried and vacuum packed before the analyses.
plant extracts using different extraction fluids. They also evaluated
the effect of water and ethanol extracts of physalis leaves at differ-
ent concentrations on lymphocyte cell proliferation to test the 2.2. Chemicals
plant’s efficacy as immunomodulator. Anh et al. (2018) isolated
bioactive compounds from the whole plant (fruit excluded) and Folin-Ciocalteau phenol reagent, 2,2-diphenyl-1-picrylhydrazyl

identified two new withanolides along with six known com- (DPPH ), ferulic acid, HPLC grade methanol, trifluoroacetic acid and
pounds, in addition to their cytotoxicity properties. Corazza et al. phenolic acids standards (gallic acid, protocatechuic acid, p-hydroxy-
(2018) evaluated the impact of extraction conditions on the benzoic acid, vanillic acid, caffeic acid, syringic acid, p-coumaric acid,
450 A.M. de Oliveira et al. / South African Journal of Botany 131 (2020) 448 453

ferulic acid and sinapic acid) were all purchased from Sigma-Aldrich
Chemical Co. (St. Louis, MO, U.S.A).
2.3. Extraction of the soluble (SF) and insoluble (IF) fractions of the
phenolic acids
P. angulata was subjected to alkaline and acid hydrolysis accord-
ing to the method reported by Mattila and Kumpulainen (2002) with
minor modifications for identification and quantification of the SF
and IF of the phenolic acids by HPLC.
2.4. Methanolic extraction
P. angulata was extrated with pure methanol according to the
method reported by de Carrasco and Zelada (2008). The extract was

used for the analysis of total phenolic compounds and DPPH radical
scavenging activity.
2.5. Total Phenolic content (TPC) determination
28 30 min,19 25% B; 30 36 min, 25 26% B; 36 38 min, 26 28%
B; 38 41 min, 28 35% B; 41 46 min, 35 40% B; 46 48 min,
40 48% B; 48 53 min, 48 53% B; 53 65 min, 53 70% B;
65 66 min, 70 9% B; and 66 70 min, 9% B. The column and the sam-
ple were maintained at 20 °C. The identification of the phenolic acids
was performed by the addition of a mixture of standards of known
concentration to the samples (spiking) based on the retention time of
the standards. The quantification of phenolic acids was based on the
differences in peak areas (spiking and standards) at a wavelength
ranging from 280 nm to 325 nm using the respective standard curves
generated from the standards of the phenolic acids.
2.8. Statistical analysis
The data were analyzed by the variance test (ANOVA) using the
statistical software SAS version 9.2 (SAS Institute Inc., Cary, NC, USA).
The Tukey test (p < 0.05) was used to report significant differences
between averages for the samples. The results were reported as
means § standard deviation.

TPC was measured using a colorimetric Folin-Ciocalteau method
(Singleton and Rossi, 1965). Gallic acid was used as a standard and
the results were expressed as mg GAE.100 g 1 lyophilized fruit.

2.6. DPPH radical scavenging activity determination

The analysis of antioxidant activity was based on the DPPH
method, described by Brand-Williams et al. (1995) and modified by
Anton et al. (2008). The results were expressed as mmol of Trolox
Equivalent Antioxidant Capacity (TEAC) per g of freeze-dried fruit.
2.7. HPLC determination
The chromatographic separation of the phenolic acids was per-
formed in the chromatograph HPLC Waters 2695 (Waters Corp., Mil-
ford, MA, USA) equipped with a photodiode array (PDA) detector
Waters 996 (Waters Corp.) and an auto-sampler Waters 717 Plus
(Waters Corp.). The analytical column used was Phenomenex one -
Gemini - C-18, 110 A (150 £ 4.60 mm - 5 mm). During the analysis,
10 mL of sample were injected by the auto sampler. The gradient
used in this study was a modification of the method described by
Guo and Beta (2013). The samples were eluted through the column
with a gradient of mobile phase A (0.1% v/v of trifluoroacetic acid
(TFA) in water) and B (0.1% v/v of TFA in methanol) under a flow rate
of 0.7 mL/min. An elution gradient of 70 min was programmed as fol-
lows: 0 11 min, 9 14% B; 11 14 min, 14 15% B; 14 17 min,
15 15% B; 17 24 min, 15 16,5% B; 24 28 min, 16,5 19% B;
3. Results and discussion
3.1. Identification and quantification of the SF and IF phenolic acids
in P. angulata fruits
A decreasing tendency in the content of phenolic acids from green
to ripe fruit was observed (Table 1), with the exception of p-coumaric
acid (SF and IF) and ferulic acid (SF). According to Gruz et al. (2011),
this result is ascribed to oxidation reactions in the SF. The decrease
may be related to the use of these acids as an energy source in the
plant respiratory process and/or as the carbon source for the synthe-
sis of sugars and other compounds. The phenolic acid profile may
also be affected by environmental, storage, processing and post-har-
vest conditions (Naczk and Shahidi, 2004).
In the SF of the green fruit, p-hydroxybenzoic acid (34.00 mg.100 g 1)
predominated among all detected phenolic acids, suffering a reduction of
94% during maturation. Lower quantities of gallic, vanillic and syringic
acids (0.70, 5.00 and 1.00 mg.100 g 1, respectively) appear in the SF of
the green fruit. Only 20% of the initial vanillic acid content was present in
the ripe fruit.
The ferulic acid was predominant in the ripe fruit of P. angulata. In
addition, this was the only acid that remained unchanged during the
fruit maturation, showing the highest concentrations in the IF for both
stages of maturation (17.00 mg.100 g 1 and 13.00 mg.100 g 1 for the
green and ripe fruits, respectively). According to Zhao and Moghada-
sian (2008), high levels of ferulic acid are found in both forms (free
and esterified) in vegetables, fruits, cereals and coffee. Similar results

Table 1
Content of phenolic acids in the soluble (SF) and insoluble (IF) fractions in both stages of maturation of P. angulata
fruits and in P. peruviana ripe fruits.

Physalis angulata L. Physalis peruviana

Phenolic acid GREEN FRUIT RIPE FRUIT RIPE FRUIT

SF IF SF IF SF IF

Gallic 0.70 ± 0.02 nd nd nd nd nd

Protocatechuic 11.00 ± 0.14 nd 0.80 ± 0.01 nd nd nd
p-hydroxybenzoic 34.00 ± 1.87 nd 2.00 ± 0.02 nd nd nd
Vanillic 5.00 ± 0.18 2.00 ± 0.06 1.00 ± 0.00 nd nd 4.00 ± 0.04
Caffeic 10.00 ± 0.06 2.00 ± 0.02 1.00 ± 0.02 2.00 ± 0.00 nd 11.00 ± 0.01
Syringic 1.00 ± 0.01 nd nd nd 3.00 ± 0.09 nd
p-coumaric 4.00 ± 0.00 1.00 ± 0.00 6.00 ± 0.05 2.00 ± 0.00 nd nd
Ferulic 9.00 ± 0.01 17.00 ± 0.01 10.00 ± 0.01 13.00 ± 0.00 5.00 ± 0.00 12.00 ± 0.02
Sinapic 9.00 ± 0.03 5.00 ± 0.01 2.00 ± 0.03 nd nd 1.00 ± 0.01
Values are presented as means ± standard deviation. The content of phenolic acids is expressed in mg.100g-1 of freeze-
dried pulp. * nd = not detected.
 A.M. de Oliveira et al. / South African Journal of Botany 131 (2020) 448 453
Table 2
TPC in the soluble (SF) and insoluble (IF) fractions in both stages of matura-
tion of fruits of P. angulata compared with fruits of P. peruviana.
Fractions Physalis angulata L. Physalis peruviana
Green Ripe Ripe
SF 798.08 § 2.87a 749.10 § 3.29a 858.18 § 3.18a
IF 2832.02 § 3.37a 3847.72 § 3.61b 3559.10 § 6.32b
Values are presented as means § standard deviation. TPC is expressed in mg
GAE.100 g 1. Different characters in the same line represent statistically sig-
nificant differences at p < 0.05.
were found by Zhang et al. (2014), whose study indicated that ferulic
acid is the predominant cinnamic acid in citrus fruits.
The data obtained for the SF and IF of the ripe fruits corroborate
with the results published by Meyer et al. (1998), which claim that
fruits represent a significant source of cinnamic acid derivatives,
largely composed of ferulic, sinapic, p-coumaric and caffeic acids.
When comparing the two species of Physalis (Table 1), it is evident
that ferulic acid was predominant in both fractions. Caffeic acid
(11.00 mg.100 g 1) was also found in significant quantities in the IF
of fruits of PP. These data differ from the results of the Rockenbach
et al. (2009), in which the ferulic acid was not detected in the free
fraction of P. peruviana and was present in the IF.

3.2. TPC and DPPH determinations in the SF and IF fractions
The ripe fruits of P. angulata showed higher TPC in the IF
(3847.72 mg.100 g 1) when compared to the green fruits (Table 2).
There was no significant difference of TPC between the two varieties
of Physalis. The sum of individual phenolic acid concentration
(Table 1) in the SF of green fruits was approximately 85 mg.100 g 1,
while the TPC in the same fraction was 798 mg 100 g 1 (Table 2). The
Folin-Ciocalteau reagent is nonspecific to phenolic compounds and
can be reduced by many nonphenolic (e.g., vitamin C, Cu(I)) com-
pounds (Huang et al., 2005), which may justify the high TPC content
found in this study.

Table 3 shows the DPPH antioxidant activity obtained in the SF
and IF of the phenolic acids extracts from fruits of P. angulata in two

maturation stages. During maturation, the values of DPPH were sim-
ilar for both fractions. In comparison to the P. peruviana fruits, the IF

from P. angulata showed a higher DPPH value (71.3%). Higher antiox-
idant activity in SF and IF of P. peruviana fruit (92.6 and 106.2 mM
TEAC.100 g 1, respectively) from the mountainous region of Rio
Grande do Sul (Brazil) was reported by Severo et al. (2010) using a
different sequential extraction from the one employed in the present
research.

3.3. TPC and DPPH determinations from the methanolic extract
Physalis is a climacteric fruit, characterized by ethylene biosynthe-
sis and an increase in respiration rate during ripening called climac-
teric peak, where there is a sudden rise in respiration rate followed
Table 3
DPPH in soluble (SF) and insoluble (IF) fractions of P. angulata fruits in
both stages of maturation compared with P. peruviana fruits.
Fractions Physalis angulata L. Physalis peruviana
Green Ripe Ripe
SF 17.60 § 13.67a 17.50 § 11.80a 16.80 § 15.21a
IF 47.10 § 10.85a 40.40 § 7.15a 28.80 § 7.71b
Values are presented as means § standard deviation. DPPH is expressed
in mM TEAC.100 g 1 of lyophilized pulp. Different characters in the same
line represent statistically significantt differences at p < 0.05.
451
Table 4
TPC and DPPH in methanolic extracts of P. angulata fruits in two
stages of maturation and in P. peruviana ripe fruits.
Samples TPC DPPH
Physalis angulata L.- green 284.17 § 0.06a 12.80 § 0.04a
Physalis angulata L.- ripe 314.84 § 0.07b 14.10 § 0.04b
Physalis peruviana - ripe 254.07 § 0.05a 11.30 § 0.01a
Values are presented by mean § standard deviation. TPC and DPPH
are expressed in mg GAE.100 g 1 and mM.TEAC.g 1 of lyophilized
pulp, respectively. Different characters in the same column repre-
sent statistically significant differences at p < 0.05.
by a decrease to reach the basal point (Prasanna et al., 2007; Ibarra-
Garza et al., 2015). Some fruits exhibit a significant decay in antioxi-
dant properties and quality over ripening due to multiple metabolic
changes. However, we have determined an increase in TPC and DPPH¢
scavenging activity over ripening. This is an important finding that
supports the potential of Physalis angulata as a functional fruit in
both local and overseas markets. The TPC content in the fruits of
P. angulata increased by 9.8% during maturation, representing a sig-
nificant difference (p < 0.05) between the two stages (Table 4). Simi-
lar results were found in fruits of P. peruviana in different maturation
stages, for which the TPC ranged from 169.19 to 210.41 mg GAE.100
g 1 (Severo et al., 2010). Valdenegro et al. (2012) also reported high
TPC levels in aqueous extract of ripe fruits of P. peruviana grown in
Chile (6.4 mg caffeic acid.100 g 1), with similar values to those
reported for fruits produced in Zagazig (Egypt) (6.3 mg caffeic
acid.100 g 1) (Ramadan and Mo € rsel 2007). The variations occurring
in the phenolic compounds during post-harvest of several fruits may
be related to biotic and abiotic stresses that induce the secondary
metabolism of the fruit, increasing, decreasing or showing irregular
behavior (Rapisarda et al., 2008).
The ripe fruits of P. angulata showed TPC 19.3% higher than the
ripe fruits of P. peruviana. The fruit of P. angulata (314.84 mg
GAE.100 g 1) also exhibited a higher TPC than that found in samples
of P. peruviana from the province of Bursa, Turkey (136.64 to
154.55 mg GAE.100 g 1) (Yıldız et al., 2015), in samples from Ecuador
(87 mg GAE.100 g 1) (Vasco et al., 2008) and in fruits from Taiwan
(19.64 to 90.80 mg GAE.100 g 1) (Wu et al., 2006).
The fruits antioxidant activity (Table 4) increased by 10.15% dur-
ing maturation. Similar behavior was determined in fruits of
P. peruviana, whose antioxidant activity increased during ripening
(Ramadan and Mo €rsel, 2007). The P. angulata DPPH’s antioxidant
capacity (12.80 and 14.10 mM TEAC.g 1 in green and ripe stages,
respectively) found in the current study is superior to those of other
fruits considered as sources of antioxidants, namely: papaya
(7.60 mM TEAC.g 1), pineapple (3.7 mM TEAC.g 1), umbu
(1.07 mM TEAC.g 1), plum (6.25 mM TEAC.g 1) and jackfruit
(0.63 mM TEAC.g 1) (Almeida et al., 2011). The antioxidant activity
may depend on several factors, such as the conditions and stages of
oxidation, formation and stability of radicals, possible location of the
antioxidants and stability at different stages of the food processing
(Szajdek and Borowska, 2008).
4. Conclusions
The HPLC analysis revealed that the phenolic acids predominant
in ripe and green fruits of P. angulata are ferulic and p-hydroxyben-
zoic. Derivatives from cinnamic acid, largely composed of ferulic,
sinapic, p-coumaric and caffeic acids, were found in both maturation
stages in fruits of Physalis, being present mostly in the soluble frac-
tion. During maturation, the P. angulata fruits showed increases of

9.8% and 10.15% in total phenolic compounds and DPPH scavenging
activity, respectively. The fruits of P. angulata showed values of TPC

and DPPH higher than those found in P. peruviana, a fruit of the
452 A.M. de Oliveira et al. / South African Journal of Botany 131 (2020) 448 453
same Solanaceae family. P. angulata fruits also exhibited antioxidant
activity substantially higher than other fruits traditionally regarded
as antioxidant, such as papaya, pineapple and plum. Considering the
phenolic acid content of P. angulata fruits, this may be considered as
a functional food with good market potential.
Declaration of Competing Interest
The authors declare no conflict of interest.
Acknowledgments
The authors are grateful for the financial support from the Natural
Sciences and Engineering Research Council of Canada (NSERC) in the
form of a Discovery Grant and the infrastructure provided by the Can-
ada Foundation for Innovation (New Opportunities Fund and Leaders
Opportunities Fund). The authors also acknowledge the Doctoral
Degree Sandwich Program from the Coordination for the Improve-
ment of High Education Personnel (CAPES, Brazil) for the financial
support. We thank Babak Sobhi (Department of Food Science, Univer-
sity of Manitoba) for the technical assistance.
References
Almeida, M.M.B., Sousa, P.H.M., Arriaga, A.M.C., ^ Prado, G.M., Magalh~aes, C.E.C,
Maia, G.A., Lemos, T.L.G., 2011. Bioactive compounds and antioxidant activity of
fresh exotic fruits from northeastern Brazil. Food Res. Int. 44, 2155–2159. https://
doi.org/10.1016/j.foodres.2011.03.051.
Anh, H.L.T., Thao, D.T., Dung, D.T., Kiem, P.V., Quang, T.H., Yen, P.T.H., Tuan, D.T.,
Cuong, P.V., Cuong, L.C.V., Hung, T.M., 2018. Phytochemical constituents and cyto-
toxic activity of Physalis angulata L. growing in Vietnam. Phytochem Lett 27, 193–
196. https://doi.org/10.1016/j.phytol.2018.07.029.
Anton, A.A., Ross, K.A., Beta, T., Gary, F.R., Arntfield, S.D., 2008. Effect of pre-dehulling
treatments on some nutritional and physical properties of navy and pinto beans
(Phaseolus vulgaris L.). LWT - Food Sci. Technol. 41, 771–778. https://doi.org/
10.1016/j.lwt.2007.05.014.
Balasundram, N., Sundram, K., Samman, S., 2006. Phenolic compounds in plants and
agri-industrial by-products: antioxidant activity, occurrence, and potential uses.
Food Chem 99, 191–203. https://doi.org/10.1016/j.foodchem.2005.07.042.
Brand-Williams, W., Cuvelier, M.E., Berset, C., 1995. Use of a free radical method to
evaluate antioxidant activity. LWT - Food Sci. Technol. 28, 25–30. https://doi.org/
10.1016/S0023-6438(95)80008-5.
Chang, L.C., Sang-Ngem, M., Pezzutto, J.M., 2016. Poha Berry (Physalis peruviana) with
potential anti-inflammatory and cancer prevention activities. Hawaii J. Med. Pub.
Health 75, 353–359.
Choi, E.M., Hwang, J.K., 2003. Investigations of anti-inflammatory and antinociceptive
activities of Piper cubeba, Physalis angulata and Rosa hybrid. J Ethnopharmacol 89,
171–175.
Corazza, G.O., Bilibio, D., Zanella, O., Nunes, A.L., Bender, J.P., Carniel, N., Santos, P.P.,
Priamo, W.L., 2018. Pressurized liquid extraction of polyphenols from Golden-
berry: influence on antioxidant activity and chemical composition. Food Bioprod.
Process. 112, 63–68. https://doi.org/10.1016/j.fbp.2018.09.001.
Dutra, R.L.T., Dantas, A.M., Marques, D.A., Batista, J.D.F., Meireles, B.R.L.A.,
Cordeiro, A.M.T.M., Magnani, M., Borges, G.S.C., 2017. Bioaccessibility and antioxi-
dant activity of phenolic compounds in frozen pulps of Brazilian exotic fruits
exposed to simulated gastrointestinal conditions. Food Res. Int. 100, 650–657.
da Silva, L.M.R., de Figueiredo, E.A.T., Ricardo, N.M.P.S., Vieira, I.G.P.,
de Figueiredo, R.W., Brasil, I.M., Gomes, C.L., 2014. Quantification of bioactive com-
pounds in pulps and by-products of tropical fruits from Brazil. Food Chem. 143,
398–404.
Fischer, G., Miranda, D., Piedrahita, W., Romero, J., 2005. Avances en cultivo, poscose-
cha y exportacion de la uchuva (Physalis Peruviana L.) en Colombia. Universidad
Nacional de Colombia, Bogota
, p. 235.
Gruz, J., Ayaz, F.A., Torun, H., Strnad, M., 2011. Phenolic acid content and radical scav-
enging activity of extracts from medlar (Mespilus germanica L.) fruit at different
stages of ripening. Food Chem. 124, 271–277. https://doi.org/10.1016/j.food-
chem.2010.06.030.
Guo, W., Beta, T., 2013. Phenolic acid composition and antioxidant potential of insolu-
ble and soluble dietary fibre extracts derived from select whole-grain cereals. Food
Res. Int. 51, 518–525. https://doi.org/10.1016/j.foodres.2013.01.008.
Ibarra-Garza, I.P., Ramos-Parra, P.A., Hern
andez-Brenes, C., Jacobo-Vela
zquez, D.A.,
2015. Effects of postharvest ripening on the nutraceutical and physicochemical
properties of mango (Mangifera indicaL. cv Keitt). Postharvest Biol. Technol. 103,
45–54.
Huang, D., Ou, B., Prior, R.L., 2005. The chemistry behind antioxidant capacity assays. J.
Agric. Food Chem. 53, 1841–1856.
Hseu, Y.C., Wu, C.R., Chang, H.W., Kumar, K.J., Lin, M.K., Chen, C.S., Cho, H.J., Huang, C.Y.,
Huang, C.Y., Lee, H.Z., Hsieh, W.T., Chung, J.G., Wang, H.M., Yang, H.L., 2011. Inhibi-
tory effects of Physalis angulata on tumor metastasis and angiogenesis. J Ethno-
pharmacol 135, 762–771.
Hsieh, W.T., Huang, K.Y., Lin, H.Y., Chung, J.G., 2006. Physalis angulata induced G2/M
phase arrest inhuman breast cancer cells. Food Chem. Toxicol. 44, 974–983.
Kusumaningtyas, R., Laily, N., Limandha, P., 2015. Potential of Ciplukan (Physalis angu-
lata L.) as source of functional ingredient. Procedia Chem. 14, 367–372. https://doi.
org/10.1016/j.proche.2015.03.050.
Leite, R.S., Hernande
z-Navarro, S., Nascimento, M.N., Potosme, N.M.R.,
Carrio
n-Prieto, P., Souza, E.S., 2018. Nitrogen fertilization affects Fourier Transform
Infrared spectra (FTIR) in Physalis L. species. Comput. Electron. Agric. 150, 411–417
. https://doi.org/10.1016/j.compag.2018.05.021.
Lorenzi, H., Matos, F.J.A., 2008. Plantas medicinais no Brasil: nativas e exo
ticas cultiva-
das, 2nd ed Instituto Plantarum, Nova Odessa.
Lusakibanza, M., Mesia, G., Tona, G., Karemere, S., Lukuka, A., Tits, M., Angenot, L.,
Fre
d e

rich, M., 2010. In vitro and in vivo antimalarial and cytotoxic activity of
five plants used in congolese traditional medicine. J Ethnopharmacol 129,
398–402.
Mattila, P., Kumpulainen, J., 2002. Determination of free and total phenolic acids in
plant-derived foods by HPLC with diode-array detection. J. Agric. Food Chem. 50,
3660–3667. https://doi.org/10.1021/jf020028p.
Mendoza, F., Aguilera, J., 2004. Application of image analysis for classification of ripen-
ing bananas. J. Food Sci. 69, 471–477. https://doi.org/10.1111/j.1365-2621.2004.
tb09932.x.
Meyer, A.S., Donovan, J.L., Pearson, D.A., Waterhouse, A.L., Frankel, E.N., 1998. Fruit
hydroxycinnamic acids inhibit human low-density lipoprotein oxidation in vitro. J.
Agric. Food Chem. 46, 1783–1787. https://doi.org/10.1021/jf9708960.
Moreira, G.C., Dias, F.S., 2018. Mixture design and Doehlert matrix for optimization of
the ultrasonic assisted extraction of caffeic acid, rutin, catechin and trans-cinnamic
acid in Physalis angulata L. and determination by HPLC DAD. Microchem. J. 141,
247–252. https://doi.org/10.1016/j.microc.2018.04.035.
Naczk, M., Shahidi, F., 2004. Extraction and analysis of phenolics in food. J. Chromatogr.
A 1054, 95–111. https://doi.org/10.1016/j.chroma.2004.08.059.
Nogueira, R.C., Rocha, V.P.C., Nonato, F.R., Tomassini, R.C.B., Ribeiro, I.M., Santos, R.R.,
Soares, M.B.P., 2013. Genotoxicity and antileishmanial activity evaluation of Physa-
lis angulata concentrated ethanolic extract. Environ. Toxicol. Pharmacol. 36, 1304–
1311.
Pietro, R.C.L.R., Kashima, S., Sato, D.N., Januario, A.H., França, S.C., 2000. In vitro antimy-
cobacterial activities of Physalis angulata. L. Phytomedicine 7, 335–338.
Puente, L.A., Pinto-Mun ~ oz, C.A., Castro, E.S., Corte

s, M., 2011. Physalis peruviana Lin-
naeus, the multiple properties of a highly functional fruit: a review. Food Res. Int.
44, 1733–1740. https://doi.org/10.1016/j.foodres.2010.09.034.
Prasanna, V., Prabha, T.N., Tharanathan, R.N., 2007. Fruit ripening phenomena an
overview. Crit. Rev. Food Sci. Nutr. 47, 1–19. https://doi.org/10.1080/
10408390600976841.
Ramadan, M.F., Moersel, J.T., 2007. Impact of enzymatic treatment on chemical compo-
sition, physicochemical properties and radical scavenging activity of goldenberry
(Physalis peruviana L.) juice. J. Sci. Food Agric. 87, 452–460. https://doi.org/
10.1002/jsfa.2728.
Rapisarda, P., Bianco, M.L., Pannuzzo, P., Timpanaro, N., 2008. Effect of cold storage on
vitamin C, phenolics and antioxidant activity of five orange genotypes [Citrus
sinensis (L.) Osbeck]. Postharvest Biol. Technol. 49, 348–354. https://doi.org/
10.1016/j.postharvbio.2008.02.002.
de Carrasco, R.R., Zelada, C.R.E., 2008. Determinacio
n de la capacidad antioxidante y
compuestos bioactivos de frutas nativas peruanas. Revista de la Sociedad Química
del Peru
74, 108–124.
Rivieira, D.A., Ocampo, Y.C., Castro, J.P., Barrios, L., Diaz, F., Franco, L.A., 2019. A
screening of plants used in Colombian traditional medicine revealed the anti-
inflammatory potential of Physalis angulata calyces. Saudi J. Biol. Sci. 26,
1758–1766.
Rockenbach, I.I., Rodrigues, E., Cataneo, C., Gonzaga, L.V., Lima, A., Mancini-Filho, J.,


Fett, R., 2009. Acidos
licos e atividade antioxidante em fruto de Physalis peruvi-
feno
ana L. Alimentos e Nutriç ~ao 19, 271–276 In Portuguese.
Rufato, L., de Rossi Rufato, A., Schlemper, C., Lima, C.S.M., Kretzschmar, A.A., 2008.
Aspectos te
cnicos da cultura da physalis 101 UFPEL/ PelotasIn Portuguese.
Rufino, M.S.M., Alves, R.E., Brito, E.S., Pe
rez-Jime
nez, J., Saura-Calixto, F., Mancini-Filho, J.,
2010. Bioactive compounds and antioxidant capacities of 18 non-traditional tropical
fruits from Brazil. Food Chem 121, 996–1002.
Silva, K.N., Agra, M.F., 2005. Estudo farmacobot^anico comparativo entre Nicandra phys-
alodes e Physalis angulata (Solanaceae). Revista Brasileira de Farmacognosia 15,
344–351. https://doi.org/10.1590/S0102-695X2005000400016 In Portuguese.
Silva, D.F., Pio, R., Soares, J.D.R., Elias, H.H.D.S., Villa, F., Boas, E.V.B.V., 2016. Light spec-
trum on the quality of fruits of physalis species in subtropical area. Bragantia 75,
371–376. https://doi.org/10.1590/1678-4499.463.
Silva, B.J.M., Pereira, S.W.G., Rodrigues, A.P.D., Nascimento, J.L.M., Silva, E.O., 2018. In
vitro antileishmanial effects of Physalis angulata root extract on Leishmania infan-
tum. J. Integr. Med. 16, 404–410.
Severo, J., Lima, C.S.M., Coelho, M.T., Rufato, A.D.R., Rombaldi, C.V., Silva, J.A., 2010. Ati-
vidade antioxidante e fitoquímicos em frutos de physalis (Physalis peruviana, L.)
durante o amadurecimento e o armazenamento. Curr. Agric. Sci. Technol. 16, 77–
82. https://doi.org/10.18539/cast.v16I1-4.2011. Portuguese.
Singleton, V.L., Rossi, J.A., 1965. Colorimetry of total phenolics with phosphomolybdic-
phosphotungstic acid reagents. Am. J. Enol. Vitic. 16, 144–158.
 A.M. de Oliveira et al. / South African Journal of Botany 131 (2020) 448 453
Sisley, G.M.M., Horna, F.Y.M., Isern, F.R., Aranda-Ventura, J., Vallejo, J.V., 2017. Actividad
inmunoestimulante del extracto acuoso liofilizado de la planta entera de Physalis
angulata L. en ratas albinas cepa Holtzman. Revista Peruana de Medicia Integrativa
2, 38–46. https://doi.org/10.26722/rpmi.2017.21.43.
Soares, M.B.P., Moema, C.B., Ribeiro, I.M., Tomassini, T.C.B., Santos, R.R., 2003. Inhibition
of macrophage activation and lipopolysaccaride-induced death by seco-steroids
purified from Physalis angulata L. Eur. J. Pharmacol. 459, 107–112.
Szajdek, A., Borowska, E.J., 2008. Bioactive compounds and health-promoting proper-
ties of berry rruits: a review. Plant Foods Hum. Nutr. 63, 147–156. https://doi.org/
10.1007/s11130-008-0097-5.
Valdenegro, M., Fuentes, L., Herrera, R., Moya-Leo
n, M.A., 2012. Changes in antioxidant
capacity during development and ripening of goldenberry (Physalis peruviana L.)
fruit and in response to 1-methylcyclopropene treatment. Postharvest Biol. Tech-
nol. 67, 110–117. https://doi.org/10.1016/j.postharvbio.2011.12.021.
Vasco, C., Ruales, J., Kamal-Eldin, A., 2008. Total phenolic compounds and antioxidant
capacities of major fruits from Ecuador. Food Chem. 111, 816–823. https://doi.org/
10.1016/j.foodchem.2008.04.054.
Wu, S.J., Tsai, J.Y., Chang, S.P., Lin, D.L., Wang, S.S., Huang, S.N., Ng, L.T., 2006. Supercriti-
cal carbon dioxide extract exhibits enhanced antioxidant and anti-inflammatory
activities of Physalis peruviana. J. Ethnopharmacol. 108, 407–413. https://doi.org/
10.1016/j.jep.2006.05.027.
View publication stats
453
Yao, L.H., Jiang, Y.M., Shi, J., Tom
as-Barber
an, F.A., Datta, N., Singanusong, R., Chen, S.S.,
2004. Flavonoids in food and their health henefits. Plant Foods Hum. Nutr. 59,
113–122. https://doi.org/10.1007/s11130-004-0049-7.
_
Yıldız, G., Izli, €
N., Unal, H., Uylaşer, V., 2015. Physical and chemical characteristics of
goldenberry fruit (Physalis peruviana L.). J. Food Sci. Technol. 52, 2320–2327.
https://doi.org/10.1007/s13197-014-1280-3.
Zamora-Tavares, M., del, P., Martínez, M., Magallo
n, S., Da
valos, L.G.,
Vargas-Ponce, O., 2016. Physalis and physaloids: a recent and complex evolu-
tionary history. Mol. Phylogenet. Evol. 100, 41–50. https://doi.org/10.1016/j.
ympev.2016.03.032.
Zhang, Y., Yujing, S., Wanpeng, X., Yan, S., Liping, Q., Liezhou, Z., Xingqian, Y., Zhiqin, Z.,
2014. Phenolic compositions and antioxidant capacities of Chinese wild mandarin
(Citrus reticulata Blanco) fruits. Food Chem. 145, 674–680. https://doi.org/10.1016/
j.foodchem.2013.08.012.
Zhang, W., Tong, W., 2016. Chemical constituents and biological activities of plants
from the genus Physalis. Chem. Biodiversity 13, 48–65. https://doi.org/10.1002/
cbdv.201500435.
Zhao, Z., Moghadasian, M.H., 2008. Chemistry, natural sources, dietary intake and phar-
macokinetic properties of ferulic acid: a review. Food Chem 109, 691–702. https://
doi.org/10.1016/j.foodchem.2008.02.039.