Postharvest Biology and Technology 67 (2012) 110117

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Postharvest Biology and Technology

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Changes in antioxidant capacity during development and ripening of goldenberry

(Physalis peruviana L.) fruit and in response to 1-methylcyclopropene treatment
Mnika Valdenegro, Lida Fuentes, Ral Herrera, Mara Alejandra Moya-Len
Laboratorio de Fisiologa Vegetal y Gentica Molecular, Instituto de Biologa Vegetal y Biotecnologa, Universidad de Talca, Casilla 747, Talca, Chile

a r t i c l e

i n f o

Article history:
Received 18 November 2011
Accepted 21 December 2011
Keywords:
Antioxidants
Goldenberry
Healthy fruit
1-MCP
Polyphenols
TEAC
Vitamin C

a b s t r a c t
Goldenberry (Physalis peruviana) is a climacteric fruit and its ripening is regulated by ethylene. Reports
indicate that the fruit contains high level of antioxidant compounds. To elucidate the role of ethylene on
the antioxidant capacity of this fruit during ripening and storage, the effect of 1-methylcyclopropene (1MCP, 0.2 L L1 ), a blocker of the ethylene receptor, and ethylene (2000 L L1 Ethrel) were tested. During
ripening of the fruit the ethylene production and respiration rates increased constantly until the end of
the process, similar to the SSC/acidity ratio. Firmness reduction started early during development and
continued throughout ripening. The measurement of total antioxidant capacity revealed a high antioxidant level in unripe fruit, and a clear increment in antioxidant capacity, ascorbic acid and polyphenol
contents was observed throughout ripening with maximum values at the ripe stage. Nevertheless, after
harvest the antioxidant capacity was rapidly reduced during the shelf-life period (20 C) and ethylene
treatment increased this reduction. Signicant preservation of the antioxidant capacity, vitamin C and
polyphenol content was observed in 1-MCP treated fruit. The results indicate that 1-MCP treatment could
be useful to preserve the high antioxidant capacity of goldenberry fruit during storage.
2012 Elsevier B.V. All rights reserved.

1. Introduction
Goldenberry or cape gooseberry (Physalis peruviana L.) is a
solanaceous plant native to tropical South America. The berry is
enclosed in a papery husk or calyx, and is around 2 cm wide, 45 g
in weight, with a smooth, orangeyellow skin and juicy pulp containing numerous small yellowish seeds. During ripening the fruit
color turns from green to orange due to chlorophyll breakdown
and carotenoid accumulation (mainly -carotene), and progressive softening occurs (Trinchero et al., 1999; Gutierrez et al., 2008).
When fully ripe, the fruit is sweet with a pleasant grape-like tang
(Morton, 1987). The fruit is eaten fresh, in salads or in cocktails, or
cooked. The fruit is very high in pectin and makes excellent pies
and jellies (Mc Cain, 1993).
Goldenberry is a climacteric fruit and shows a clear rise
in ethylene production during ripening (Trinchero et al., 1999;
Majumder and Mazumdar, 2002; Gutierrez et al., 2008). Ethylene plays an important role in the ripening process of climacteric
fruit (Abeles et al., 1992), initiating and enhancing ripeningrelated changes, including esh rmness reduction, soluble solids
increase, avour enhancement and autocatalytic ethylene production (Watkins, 2002). The treatment of several climacteric fruit
with 1-methylcyclopropene (1-MCP), a strong inhibitor of ethylene

Corresponding author. Tel.: +56 7120 0280; fax: +56 7120 0276.
E-mail address: alemoya@utalca.cl (M.A. Moya-Len).
0925-5214/$ see front matter 2012 Elsevier B.V. All rights reserved.
doi:10.1016/j.postharvbio.2011.12.021

action, has been shown to inhibit ethylene production, delay fruit

softening and inhibit the production of aroma volatile compounds
(Watkins, 2002; Blankenship and Dole, 2003). The application of
1-MCP (0.5 and 5 L L1 ) to goldenberry fruit at different ripening stages has been reported showing that 1-MCP either delays
the onset of the ethylene climacteric at the initial ripening stages
or transiently decreases ethylene production at a more advanced
ripening stage (Gutierrez et al., 2008).
Goldenberry is one of the most promising of tropical fruit due
to its rapid growth and high yield (Morton, 1987; Mc Cain, 1993). A
single plant may yield 300 fruit and carefully tended plants can provide about 33 ton ha1 . In addition to having a commercial future
as an exotic fresh fruit, the general chemical composition of goldenberry has many medicinal and edible uses (Morton, 1987; Mc
Cain, 1993; Ramadan and Mrsel, 2009; Ramadan, 2011a,b). The
fruit contains high levels of nutritional and antioxidant compounds,
with the pulp containing vitamins A, B and C, -carotene, phosphorus and iron (Hewett, 1993; Wu et al., 2005; Ramadan and Mrsel,
2007). Plant extracts show antioxidant activity (Chang et al., 2008),
as well as anti-hepatotoxic (Arun and Asha, 2007), antiproliferative
effects on hepatome cells (Wu et al., 2004) and anti-inammatory
activity (Wu et al., 2006). In addition, it has excellent potential as a
food-based strategy as antidiabetes and antihypertension solutions
(Pinto et al., 2009).
Oxidative damage in the human body plays an important
causative role in disease initiation and progression (Yamaguchi
et al., 1998). Damage is generally reduced by endogenous

M. Valdenegro et al. / Postharvest Biology and Technology 67 (2012) 110117

antioxidants, but additional protection is necessary, and therefore

nutritive elements from food are critical in disease prevention.
Vitamin antioxidants in food include vitamin C (ascorbic acid,
AA), -carotene and -tocopherol. Vitamin C is the water-soluble
antioxidant most abundant in blood (Kinsella et al., 1993). Many
clinical and epidemiological studies have sought to demonstrate
the efcacy of these vitamins in preventing a wide variety of
diseases (Blumenthal et al., 2000; Giugliano, 2000; Haegele et al.,
2000). However, some in vitro studies (Pellegrini et al., 2000;
Scheen, 2000) suggested that vitamins obtained via whole food
or by a balanced diet may be more effective than supplements,
possibly through synergistic interactions with other compounds.
The role of AA is to reduce hydrogen peroxide (H2 O2 ), which
preserves cells against reactive oxygen species (Davey et al.,
2000; Kleszczewska, 2000). Humans are not able to synthesize AA
(Kleszczewska, 2000), and therefore the only human source is food
(Englard and Seifter, 1986). The main sources of AA are fruit and
vegetables, especially citrus fruit, strawberries, peppers, tomatoes,
cabbage, and spinach (Davey et al., 2000).
A high antioxidant capacity has been demonstrated for goldenberry juice (Ramadan and Mrsel, 2007) and the synergistic effect of
different antioxidants has been suggested. Also a high level of phenolic compounds was reported for the fruit (Ramadan and Mrsel,
2007). Phenolic compounds seem to be mainly responsible for the
antioxidant activity of fruit juices and wines (Frankel et al., 1995;
Wang et al., 1996; Miller and Rice-Evans, 1997), whereas AA seems
to play a minor role. According to Wang et al. (1996), less than 15% of
total antioxidant activity of a fruit is due to vitamin C. The stronger
antioxidant capacity of many phenols and polyphenols compared
to vitamin antioxidants has been conrmed. Phenolic compounds
have been associated with a lowered risk of heart disease via their
action towards low-density lipoproteins (LDL) (Vinson et al., 2001).
On the other hand, phenolics are also important because of their
contribution to the sensory quality of fruit (colour, astringency, bitterness and avour). Finally, the total content of antioxidants in a
fruit depends on the species and cultivar, and can be affected by
many factors such as environmental conditions of growing, harvest
time, ripening stage, storage and processing conditions.
As goldenberry is a promising fruit with a high level of antioxidant capacity (Ramadan, 2011a,b), the objective of this work was to
examine the level of antioxidants during ripening development of
the fruit and during its shelf-life. In addition, the effect of ethylene
and 1-MCP treatments at a low concentration (0.2 L L1 ) on the
antioxidant capacity of goldenberry fruit was investigated in depth
for the rst time.

2. Materials and methods

2.1. Plant material and treatments
Goldenberry fruit (P. peruviana) were hand-picked from a commercial eld located at Huaqun, Maule Region, Chile (35 05 S;
71 44 W; 87 masl). Plants in the eld correspond to a Colombian Physalis cultivar imported to Chile as seeds and vegetatively
propagated by farmers. Two harvests were performed in two consecutive seasons: 4th May 2008 and 18th May 2009. The fruit were
dehusked and then uniform fruit without defects were classied
into 5 different ripening stages according to Trinchero et al. (1999):
IG, immature fruit stage, small green berry with fresh calyx; MG,
mature green stage, greenyellow fruit covered by greenish to pale
yellow calyx; Y, yellow stage, dark yellow berry with calyx not
completely dry; OR, orange ripe stage, light orange and large fruit
covered by light brown, dry and paper-like calyx; OO, orange overripe stage, large orange fruit with manifested softening covered by
a brown and dry calyx.

111

In the rst season, fruit at the yellow or orange stage was divided
at random into three groups. The rst group was subjected to 1MCP application at 0.2 L L1 1-MCP (SmartFreshTM ) during 12 h
at 20 C (Moya-Len et al., 2006) and then ventilated for 3 h, while
the second group was treated with ethylene, by dipping the fruit
in a 2000 L L1 EthrelTM solution for 3 min and subsequent drying (Balbontn et al., 2007). A third group remained untreated as
control fruit. Each fruit group was stored at 20 C 1 C for up to
14 d and samples were taken every 5 d. In the second season, the
fruit were divided in two groups: 1-MCP treatment and control
fruit. The fruit were stored at 20 C 1 C for up to 6 d and samples
were taken every 2 d. After quality assessments the fruit were cut
into small pieces, frozen under liquid nitrogen and stored at 80 C
until use. Three replicates of ten fruit each were employed for each
treatment to perform ripening assessments (esh rmness, soluble solids, acidity, ethylene and respiration rate), and antioxidant
capacity, total phenols and vitamin C determinations.
2.2. Fruit quality assessment
Fruit rmness was measured using the Firm Tech II equipment
(Bio Works Inc., USA) provided with a at tip of 2 cm. Two measurements on each equatorial side were performed on each fruit.
The mean of each replicate (10 fruit per stage or treatment) was
recorded and expressed as newtons (N) standard error (SE).
After the rmness measurement, the fruit was cut into pieces
and frozen under liquid nitrogen and stored at 80 C until use. 2 g
of fruit tissue from each replicate were homogenized in water in
a warring blender and adjusted to 25 mL nal volume. The mixture was ltrated through miracloth and the juice was analyzed for
soluble solids concentration (SSC), pH, and titratable acidity (TA).
SSC was determined at 20 C using a hand-held temperature compensated refractometer (Atago Co., Tokyo, Japan), and expressed
as g g1 of fresh weight (FW). TA was determined by titration of
an aliquot of 5 mL of juice with 20 mM NaOH until reaching pH
8.2 with a pH meter (Pasco Scientic, PS-2117) and expressed as
milliequivalents of citric acid per g FW. SSC/acidity ratio was then
calculated.
The amount of fruit collected from the IG stage on the rst season
and from the OO stage on the second season was not enough to
fulll the replicates required for quality assessments, and as the
assessments were performed on only one replicate the data are not
reported (see Fig. 1).
2.3. Ethylene production and respiration rates
Three replicates of approximately 20 g of intact fruit were
introduced into close tight chambers (400 mL) and incubated at
20 C for 2 h. 1 mL gas samples were withdrawn from the headspace
volume of the chambers and quantied for ethylene in a Perkin
Elmer (Clarus 500) Gas Chromatograph, equipped with a ame ionisation detector and an Elite Plot Q column (30 m 0.32 mm i.d.)
at 80 C, using helium as a carrier gas (50.3 cm s1 ). Injector and
detector temperatures were 120 C and 155 C, respectively. Three
independent ethylene samples were taken per chamber and results
were expressed as means (nL g1 h1 ). Ethylene samples of known
concentration (4 L L1 ) were routinely used for equipment calibration. Then the needle of a CO2 detector (MAP Headspace Gas
Analyzer, Bridge Analyzers, USA) was introduced into the same
chambers and CO2 concentrations were recorded. Respiration rates
were expressed as mg CO2 kg1 h1 .
2.4. Measurement of total antioxidant activity
The standard Trolox equivalent antioxidant capacity (TEAC)
assay was used to determine total antioxidant activity (Van den

M. Valdenegro et al. / Postharvest Biology and Technology 67 (2012) 110117

2,0
100
Ethylene
Respiration
Firmness

1,5

MG

OR

1,5

30

1,0

20

0,5

10
SSC
Acidity
SSC/acidity

MG

OO

Fruit stage
4,0

OO

2,5

2,0
100
Ethylene
Respiration
Firmness

1,5

1,0
OR

Fruit stage

Firmness (N)

200

-1

-1

3,0

2,0

-1

SSC (g gFW ); Acidity (meq gFW )

-1

Ethylene production rate (nL g h )

-1 -1
Respiration rate (mg Kg h )

3,5
300

OR

50

MG

Fruit stage

400

IG

0,0

1,0

40

SSC/acidity ratio

2,5

200

Firmness (N)

3,0

-1

-1

3,5
300

2,0

-1

SSC (g gFW ); Acidity (meq gFW )

-1

Ethylene production rate (nL g h )

-1 -1
Respiration rate (mg Kg h )

50

4,0

400

40

1,5

30

1,0

20

0,5

10

SSC
Acidity
SSC/acidity

SSC/acidity ratio

112

0,0

IG

MG

OR

Fruit stage

Fig. 1. Changes in ripening indices during development of goldenberry fruit. Fruit harvested in season 2008 (A and B) and season 2009 (C and D) were classied into different
ripening stages and used in fruit quality and ripening assessments. Data correspond to means SE of three replicates of ten fruit.

Berg et al., 1999; Murcia et al., 2009). It measures the ability of

antioxidants to quench the 2,2-azino-bis(3-ethylbenzothiazoline6-sulfonic acid) radical anion (ABTS ) in both lipophilic and
hydrophilic environments. The ABTS radical solution was
generated by incubating a mixture of 2.5 mM 2,2-azobis(2amidinopropane) hydrochloride (ABAP) and 20 mM ABTS solution
in 100 mL of PBS buffer (100 mM phosphate and 150 mM NaCl, pH
7.4) at 60 C for 12 min protected from light and then stored at
room temperature. Absorbance at 734 nm was measured to check
ABTS formation (absorbance must be between 0.35 and 0.45).
10 g of frozen sample were ground in 10 mL of PBS buffer, and 40 L
of the homogenate was mixed with 1.96 mL of the radical solution. The decrease in absorbance at 734 nm was recorded during
6 min and used to calculate TEAC. A calibration curve was prepared
with different concentrations of Trolox, a water-soluble analogue
to vitamin E, in the concentration range 0.050.5 mM. TEAC values
represent the concentration of Trolox that has the same antioxidant capacity of the analysed sample. TEAC values were calculated
according to Murcia et al. (2004) and the results were expressed as
Trolox equivalents per kg FW. Determinations were performed at
room temperature in triplicate.

and then separated through a reverse-phase C18 analytical column (Kromasil 100, 25 cm 4.6 mm 5 m), equipped with a C18
precolumn (Kromasil) thermostatized at 35 C with a ow rate of
0.7 mL min1 . The chromatography was carried out using an Agilent
1100 series HPLC system provided by a photodiode array detector
(DAD) equipped with a manual injector (20 L injection volume)
and interfaced to a PC running ChemStation chromatography manager software (Hewlett-Packard).
For elution, a linear gradient was prepared from 100% solution
A (20 mM ortho-phosphoric acid in water) to 100% solution B (95%
methanol) in 10 min. The absorbance at 254 nm was recorded with
a UVvis detector. A standard curve in the concentration range
10100 mg ascorbic acid was used. DHA was quantied after its
reduction into Asc by dithiothreitol (DTT). For that, samples were
incubated for 24 h at room temperature in the presence of 1 mM
DTT, and then subjected to a new HPLC separation and quantication in which values correspond to total vitamin C content (Pavet
et al., 2005; Vanacker et al., 2006). DHA content corresponds to the
difference between total vitamin C and Asc. Values were expressed
as mg ascorbic acid per 100 g FW. Determinations of each biological
replicate were performed in quadruplicate and data correspond to
mean SE.

2.5. Determination of ascorbate, dehydroascorbate and vitamin C

contents

2.6. Determination of total phenols

Ascorbate (Asc) and dehydroascorbate (DHA) contents in the

supernatant were determined by HPLC according to Wimalasiri and
Wills (1983) with minor modications. 5 g of frozen sample were
ground in 10 mL of cold 5% phosphoric acid, and adjusted to 50 mL
nal volume with the same solution. The nal solution was kept
on ice in darkness for 30 min and then centrifuged at 20,000 g for
25 min. The supernatant was cleaned through a 0.2 m nylon lter

The total phenol content was measured by the Folin-Ciocalteu

reagent using caffeic acid as standard (Galati et al., 2003). 1 mL of
fruit juice was mixed with 5 mL of Folin-Ciocalteau reagent (previously diluted 30-fold with distilled water) and 15 mL of 0.2 g mL1
sodium bicarbonate, and then the mixture was adjusted to 100 mL
with distilled water. The solution was kept in the dark at room temperature for 2 h, and the absorbance recorded at 760 nm. The mean

M. Valdenegro et al. / Postharvest Biology and Technology 67 (2012) 110117

value of total phenolics content was obtained from cuadruplicate

measurements of biological replicates and results were expressed
as mg caffeic acid per 100 g FW.
2.7. Statistical analysis
The experiments were conducted using a complete random
design with three replicates. Statistical analyses were performed
using the SPSS v.14 package. Analysis of variance was performed
and signicant differences were determined at P 0.05 (LSD test
for quality assessment).

113

during development and ripening of the fruit. Firmness reduction started early during development (MG stage) and continued
during ripening development. Similar physiological trends for goldenberry fruit were recorded in two consecutive seasons, and they
are comparable to the changes reported by Gutierrez et al. (2008),
conrming the climacteric behaviour of the fruit. Nevertheless, differences in respiration trends were observed compared to Gutierrez
et al. (2008), as they indicate a constant reduction in respiration
as the fruit ripens. Goldenberry fruit is characterized by a high
ethylene production rate in addition to a high respiration rate.
3.2. Effect of 1-MCP on ripening physiology of goldenberry fruit

3. Results and discussion

3.1. Ripening development of goldenberry fruit
Fruit at each harvest were classied using the same criteria
reported by Trinchero et al. (1999). According to that, fruit from
the IG and MG stages correspond to developing fruit, while fruit
from the Y, OR and OO stages correspond to ripening fruit.
During fruit ripening, a reduction in rmness and acidity, and
an increase in SSC took place (Fig. 1), while ethylene was being
profusely produced. During transition from MG to Y stages, a clear
increase in ethylene production was observed (23-fold increment)
and a similar pattern was recorded for SSC. Ethylene production
increased constantly until the end of ripening. Respiration of the
fruit also increased during ripening development. Acidity diminished during ripening, with a clear reduction between the transition
from Y to OR stages. The SSC/acidity ratio increased constantly

Fruit harvested at the Y stage showed a rapid decrease in rmness during shelf-life, and a constant increase in the SSC/acidity
ratio (Fig. 2). Respiration rate of detached fruit displayed a small
increase during the rst 2 d of shelf-life, but decreased after that,
similar to the ethylene behaviour that increased until day 3,
decreasing thereafter. Similar rmness and ethylene trends were
previously described in detached Y stage fruit (Gutierrez et al.,
2008). The treatment of fruit with 0.2 L L1 1-MCP slowed down
the ethylene climacteric phase, and also the changes in rmness
and SSC/acidity ratio. Ethylene production rate of 1-MCP treated
Y-stage fruit increased slowly during shelf-life until day 5, reaching
maximum values much lower than in non-treated fruit, and then
decreased until the end of the observation period (Fig. 2). Similar
ethylene effects were previously described with higher 1-MCP
concentrations (Gutierrez et al., 2008). The respiration rate of
1-MCP treated fruit did not show the transient increase observed

Fig. 2. Development of ripening indices during shelf-life of goldenberry fruit after different postharvest treatments. Goldenberry fruit from season 2008 were harvested at the
yellow stage and then treated with 1-MCP (0.2 L L1 ), Ethrel (2000 L L1 ), or remained untreated (control), and then left at 20 C during the shelf-life period. Determinations
were performed in triplicate and data correspond to mean SE of three replicates of ten fruit.

114

M. Valdenegro et al. / Postharvest Biology and Technology 67 (2012) 110117

Table 1
Development of ripening indices during shelf-life of goldenberry fruit harvested at the yellow (Y) and orange (OR) stages and subjected to different postharvest treatments.
Ripening index

Shelf-life period (days)

Y stage

OR stage

Control

1-MCP treatment

Firmness (N)

0
2
4
6

3.8
2.7
2.7
2.6

0.3a
0.3ab
0.3ab
0.2b

3.8
3.4
2.9
2.6

0.3a
0.4a
0.2ab
0.2b

TSS (g gFW1 )

0
2
4
6

11.5
12.5
12.7
13.3

0.2a
0.6a
0.2a
0.9a

11.5
11.7
11.5
12.7

Acidity (meq gFW1 )

0
2
4
6

55.6
36.3
47.6
39.7

2.7a
7.2b
8.0ab
7.1b

55.6
24.9
28.7
28.8

Respiration rate (mg CO2 kg1 h1 )

0
2
4
6

109.1
126.6
83.6
54.6

28.5a
10.2a
13.9b
8.2c

Ethylene production rate (nL g1 h1 )

0
2
4
6

203.3
261.2
129.1
138.4

9.7b
11.0a
2.6c
0.1b

Control

1-MCP treatment

3.0
2.3
2.3
2.3

0.4a
0.3b
0.3b
0.2b

3.0
2.9
2.7
2.6

0.4a
0.3a
0.3a
0.2ab

0.2a
0.8a
1.5a
1.1a

14.8
13.1
9.0
12.9

0.2a
1.0b
1.9bc
0.9b

14.8
11.9
13.1
12.8

0.2a
1.3b
0.4b
0.3b

2.7a
1.8c
3.0c
5.5c

40.9
24.0
22.4
30.2

2.2a
1.2c
1.5c
6.1b

40.9
25.9
26.2
27.5

2.2a
2.8bc
3.4b
0.8b

109.1
54.2
57.1
18.9

28.5a
25.7c
9.4c
6.1e

109.1
135.0
127.8
106.4

28.5a
7.6a
22.0a
23.5a

109.1
83.6
72.9
63.5

28.5a
15.2ab
5.7b
9.3b

203.3
82.4
88.9
94.5

9.7b
3.3e
1.8e
1.9d

204.0
190.0
129.1
138.4

9.8a
7.6b
2.6d
0.1d

204.0
123.8
150.0
153.0

9.8a
5.0d
3.0c
3.1c

Goldenberry fruit collected on May 2009 at the yellow (Y) or orange (OR) stages were treated with 1-MCP (0.2 L L1 ) or remained untreated (control). Ripening assessments
were performed every 2 d and data correspond to mean SE of three replicates of ten fruit. Different letter for the same ripening index indicates signicant differences by
ANOVA (P < 0.05).

in non-treated fruit during the rst days of shelf-life. On the other

hand, ethylene treatment accelerated the changes in the fruit,
reaching in less than 5 d the condition of control fruit after 10 or
15 d. In addition, ethylene treatment also increased the maximum
ethylene production and the respiration rates of the fruit.
The treatment of goldenberry fruit with 1-MCP at a more
advanced ripening stage (OR) was not as effective as its application at the Y stage, nevertheless a slow down in rmness, acidity
and ethylene changes was observed (Table 1). It can be concluded
that 1-MCP application prevents degradation of goldenberries and
that its effectiveness is higher in fruit at the initial stages of the
climacteric phase than in a more advanced stage.
3.3. Antioxidant level during ripening of goldenberry fruit
Measurements of total antioxidant activity (TEAC) indicated
that goldenberry fruit have high levels of antioxidants at all
developmental and ripening stages (Fig. 3). The levels increased
markedly during ripening, with maximum values at the OR and
OO stages (Table 2). Higher TEAC levels were determined in fruit
from harvest 1. In detached fruit, the antioxidant level was rapidly
reduced during the storage period. Signicant antioxidant level
retention was observed in 1-MCP treated fruit, especially at harvest
2. On the other hand, ethylene treatment induced a rapid reduction
in total antioxidant levels.
The levels of ascorbic acid and vitamin C increased during ripening development and signicant changes were recorded between
the different stages (Fig. 4), with maximum values at the OR and
OO stages. Similar ascorbic acid levels were previously indicated
for goldenberry fruit (Gutierrez et al., 2008), and although the
increase in ascorbic acid content was observed when IG and OR
stages were compared, non-signicant increments were reported
between different ripening stages. In detached fruit, the levels of
ascorbic acid and vitamin C were rapidly reduced during storage
at 20 C (Table 3), and ethylene exacerbated the reduction of them.
Nevertheless, 1-MCP treatment avoided the fast changes and the
fruit retained high levels of ascorbic acid and vitamin C during

storage. These results suggest that 1-MCP allows the retention of a

higher antioxidant capacity by the fruit, similar to the data reported
in apricot (Egea et al., 2010) and peach (Flores et al., 2008). In
mangoes, the treatment of 1-MCP also reduced ascorbic acid losses
during shelf-life (Alves et al., 2004; Islas-Osuna et al., 2010), helping to maintain fruit nutritional value. Nevertheless, Gutierrez et al.
(2008) reported that 1-MCP did not affect signicantly ascorbic acid
changes in goldenberry fruit.
The level of ascorbic acid determined in goldenberry fruit
grown in Chile was 32 mg 100 g1 , which is similar to the values
reported by Ramadan (2011a) (43 mg 100 g1 ) for fruit produced
in Colombia. Ascorbic acid level in goldenberry fruit is higher than
in fruit like pear (4 mg 100 g1 ), apple (6 mg 100 g1 ), peach (7 mg
100 g1 ), and comparable with orange (50 mg 100 g1 ) and strawberry (60 mg 100 g1 ) (Belitz and Grosch, 1999).
The content of total phenolic compounds increased during
development and ripening of (Fig. 3), with maximum values in
fully ripe fruit (OR and OO stages). A high level of phenolic compounds was determined in ripe goldenberry fruit grown in Chile
(around 6.4 mg 100 g1 ), which is similar to the values reported previously (6.3 mg 100 g1 ) for fruit produced in Colombia (Ramadan
and Mrsel, 2007). During the storage of detached fruit at 20 C, a
small decrease in the content of phenolic compounds was observed
(Table 3). The treatment of fruit with ethylene stimulated the loss
of phenolic compounds, while 1-MCP treatment maintained a high
level of them during longer storage times.
Similar trends were recorded for total antioxidant activity and
phenols during ripening, and also in response to 1-MCP. This is not
surprising as the Folin-Ciocalteau reagent (FCR) method and TEAC
assay are based on equivalent chemical principles (Huang et al.,
2005). The FCR based assay measures the reducing capacity of a
sample, albeit it is known as the total phenolic assay. The high level
of phenolic compounds found in goldenberry fruit could be protecting ascorbic acid oxidation, by the protective effect of polyphenols
(Miller and Rice-Evans, 1997).
Goldenberry fruit is considered to display a long postharvest life,
as it can be stored for several months in a dry atmosphere without

M. Valdenegro et al. / Postharvest Biology and Technology 67 (2012) 110117

115

Table 2
Effect of 1-MCP and ethylene treatments in the antioxidant level of Physalis peruviana fruit.
Ripening stage

TEAC valuea

Treatment

Shelf-life period (days)

Control
1-MCP
Ethylene
Control
1-MCP
Ethylene
Control
1-MCP
Ethylene

0
6.87 0.10a
6.87 0.10a
6.87 0.10a
7.67 0.04a
7.67 0.04a
7.67 0.04a
8.67 1.04a
8.67 1.04a
8.67 1.04a

5
6.42 0.31b
6.75 0.34a
6.02 0.17b
7.32 0.12b
7.01 0.32b
6.12 0.27e
8.39 0.89ab
7.99 0.31b
6.31 0.65c

10
6.34 0.42b
6.28 0.31b
5.66 0.16c
7.26 0.27b
7.09 0.49b
5.87 0.10e
8.21 0.86ab
7.82 0.51b
6.22 0.33c

14
6.28 0.32b
6.10 0.15b
5.21 0.37d
7.02 0.1c
6.89 0.06d
5.42 0.03f
8.06 0.18b
7.69 0.34b
5.64 0.25c

Control
1-MCP
Control
1-MCP
Control
1-MCP

0
6.21 0.18a
6.21 0.18a
6.23 0.25a
6.23 0.25a
6.34 0.31a
6.34 0.31a

2
5.45 0.18b
6.21 0.14a
5.80 0.09b
6.23 0.22a
6.19 0.15b
6.34 0.26a

4
5.38 0.18b
6.21 0.16a
5.80 0.09b
6.22 0.28a
6.19 0.14b
6.34 0.31a

6
5.24 0.18b
6.20 0.12a
5.80 0.12b
6.23 0.21a
6.19 0.17b
6.33 0.27a

Harvest 1
Yellow

Orange

Overripe

Harvest 2
Yellow
Orange
Overripe

Goldenberry fruit were collected on May 2008 (Harvest 1) and May 2009 (Harvest 2). Fruit from the Y, OR and OO stages were treated with 1-MCP (0.2 L L1 ), or with Ethrel
(2000 L L1 ), or remained untreated (control). After treatment, fruit was left at 20 C during the shelf-life period. Determinations were performed in triplicates and data
correspond to mean SE of three replicates of ten fruit. Different letters at the same ripening stage indicate signicant differences between treatments by ANOVA (P < 0.05).
a
TEAC equivalents correspond to the antioxidant capacity of a Trolox solution: Trolox solution of 0.05 mM, TEAC value of 1; 0.25 mM, TEAC value of 5; 0.50 mM, TEAC
value of 10. TEAC values were expressed as Trolox equivalents per kg FW.

6,4

TEAC
C value

6,2
6,0

5,8
5
8
4

5,6
TEAC

Phenols

5,4

Total phenols ((mg 100gFW-1)

6,6

10

5,2
5,0

0
IG

MG

OR

OO

Fruit stages
10

-1

6,4

8
6,2

TEAC value

Total phenols
s (mg 100gFW )

6,6

6,0

5,8
4

5,6
5,4

TEAC
Phenols

5,2
50
5,0

IG

MG

OR

OO

Fruit stages
Fig. 3. Changes in the antioxidant level (scavenging of ABTS radical anions) and
total phenolic compounds during ripening of goldenberry fruit. Fruit were collected
on May 2008 (A) and May 2009 (B), and classied into different ripening stages.
Determinations were performed in triplicate and data correspond to means SE of
three replicates. TEAC values were expressed as Trolox equivalents per kg FW. TEAC
equivalents correspond to the antioxidant capacity of the following Trolox solutions:
0.05 mM, TEAC value of 1; 0.25 mM, TEAC value of 5; 0.50 mM, TEAC value of 10.

Fig. 4. Changes in ascorbic acid (Asc), dehydroascorbic acid (DHA) and vitamin C (Vit
C) content during ripening of goldenberry fruit. Fruit were collected on May 2008 (A)
and May 2009 (B), and classied into different ripening stages. Determinations were
performed in quadruplicate and data correspond to means SE of three replicates.

116

M. Valdenegro et al. / Postharvest Biology and Technology 67 (2012) 110117

Table 3
Effect of 1-MCP and ethylene treatments in the content of ascorbic acid, dehydroascorbic acid, vitamin C and total phenolic compounds (mg per 100 gFW) in Physalis peruviana
fruit.

Harvest 1

Ripening stage

Days

Treatment

Ascorbic acid

Dehydroascorbic acid

Vitamin C

Total Phenols

Yellow

Control
1-MCP
Ethylene
Control
1-MCP
Ethylene
Control
1-MCP
Ethylene
Control
1-MCP
Ethylene
Control
1-MCP
Ethylene
Control
1-MCP
Ethylene
Control
1-MCP
Ethylene
Control
1-MCP
Ethylene
Control
1-MCP
Control
1-MCP
Control
1-MCP
Control
1-MCP
Control
1-MCP
Control
1-MCP
Control
1-MCP
Control
1-MCP

28.58 0.56a
28.58 0.56a
28.58 0.56a
20.05 0.31b
24.89 0.89a
17.43 0.67b
18.31 0.42b
20.65 1.20b
15.44 0.34c
13.24 0.26c
17.83 0.56b
12.02 0.75c
31.24 0.41a
31.24 0.41a
31.24 0.41a
22.45 0.56b
26.74 0.32b
23.45 0.61b
20.31 0.78c
24.10 0.40b
17.45 0.35c
18.31 0.56c
20.62 0.77c
13.71 0.81d
31.65 0.42a
31.65 0.42a
23.45 0.12b
28.98 0.33a
19.37 0.29b
28.44 0.21a
13.05 0.06c
24.56 0.32b
28.65 0.32a
28.66 0.33a
26.36 0.21a
25.54 0.32a
20.22 0.67b
21.87 0.43b
19.05 0.43b
20.54 0.65b

4.27 0.78a
4.27 0.78a
4.27 0.78a
3.12 0.85b
4.09 0.54a
3.27 0.38b
2.26 0.52c
3.31 0.84b
2.20 0.61c
2.11 0.65c
3.02 0.76b
2.00 0.52c
3.76 0.99a
3.76 0.99a
3.76 0.99a
2.77 0.22c
3.35 0.19b
2.78 0.08c
3.05 0.83b
2.88 0.51c
2.53 0.47c
2.76 0.33c
2.62 0.27c
2.31 0.18c
2.98 0.23a
2.98 0.23a
2.70 0.56a
3.10 0.77a
2.30 0.05b
2.90 0.21a
1.87 0.45b
2.77 0.19a
2.21 0.12a
2.22 0.13a
3.13 0.09a
2.61 0.06a
2.80 0.31a
2.90 0.99a
2.20 0.54b
2.62 0.28a

32.85 0.53a
32.85 0.53a
32.85 0.53a
23.17 0.24b
28.98 0.18b
20.70 0.12c
17.57 0.51c
23.96 0.24c
17.64 0.43c
15.35 0.33d
20.85 0.27c
14.02 0.15d
35.00 0.12a
35.00 0.21a
35.00 0.16a
25.22 0.31c
30.09 0.44b
26.23 0.23c
25.41 0.17c
28.36 0.53b
19.98 0.32d
23.07 0.21c
23.24 0.18c
16.02 0.42d
34.69 0.37a
34.69 0.37a
26.15 0.32b
32.08 0.21a
21.67 0.10b
31.34 0.21a
14.92 0.35c
27.33 0.27b
30.86 0.22a
30.87 0.29a
29.49 0.33a
28.15 0.26a
23.02 0.31b
24.77 0.27b
21.25 0.35b
23.16 0.31b

6.12 0.10a
6.12 0.10a
6.12 0.10a
6.10 0.09a
6.12 0.01a
6.04 0.01b
6.03 0.02b
6.11 0.05a
6.05 0.01b
6.00 0.07b
6.10 0.02a
5.88 0.02c
6.45 0.06a
6.45 0.06a
6.45 0.06a
6.41 0.01b
6.44 0.01b
6.32 0.01c
6.12 0.02c
6.24 0.01c
6.07 0.01c
6.02 0.01d
6.16 0.01c
5.87 0.03d
5.86 0.11a
5.86 0.11a
5.82 0.12a
5.81 0.08a
5.77 0.04b
5.77 0.03b
5.60 0.05c
5.70 0.04c
5.55 0.08a
5.63 0.04a
5.43 0.02b
5.58 0.02a
5.42 0.05b
5.60 0.06b
5.31 0.04b
5.61 0.06b

10

14

Orange

10

14

Harvest 2

Yellow

0
2
4
6

Orange

0
2
4
6

Goldenberry fruit was collected on May 2008 (Harvest 1) and May 2009 (Harvest 2). Fruit from the yellow and orange stages were treated with 1-MCP (0.2 L L1 ), Ethrel
(2000 L L1 ), or remained untreated (control), and then left at 20 C during the shelf-life period. Determinations were performed in triplicates and data correspond to
mean SE of three replicates of ten fruit. For a particular compound, different letters at the same harvest and ripening stage indicate signicant differences by ANOVA
(P < 0.05).

special storage conditions. However, these studies only consider

external quality and do not pay attention to nutritional and health
properties. Therefore, in order to obtain a goldenberry fruit with a
high antioxidant level and better nutritional quality, it is important
to harvest at the ripe stage and to avoid storage for long periods as
its health properties deteriorate with time.
In conclusion, goldenberry fruit is a climacteric fruit characterized by a high ethylene production rate. Ethylene induces several
ripening events. During ripening of the fruit the level of antioxidants and phenolic compounds increases, however in detached
fruit a signicant reduction is observed. The treatment of fruit with
1-MCP (0.2 L L1 ) slowed down the degradation of the fruit, and
preserved antioxidants and phenolic compounds at a high level for
longer periods. Finally, it can be concluded that goldenberry fruit
is a good source of bioactive compounds and its use as a functional
food deserves further study.

Acknowledgements
This work has been partly supported by PBCT (Programa Bicentenario de Ciencia y Tecnologa) Anillo ACT-41 and Postdoctoral
PSD-61 Projects.

References
Abeles, F.B., Morgan, P.W., Salveit, M.E., 1992. Ethylene in Plant Biology, second ed.
Academic Press, London.
Alves, R.E., Filgueiras, H.A.C., Almeida, A.S., Pereira, M.E.C., Cocozza, F.M., Jorge,
J.T., 2004. Postharvest ripening of Tommy Atkins mangoes on two maturation
stages treated with 1-MCP. Acta Hort. (ISHS) 645, 627632.
Arun, M., Asha, V.V., 2007. Preliminary studies on antihepatotoxic effect of Physalis
peruviana Linn (Solanaceae) against carbon tetrachloride induced acute liver
injury in rats. J. Ethnopharmacol. 111, 110114.
Balbontn, C., Gaete-Eastman, C., Vergara, M., Herrera, R., Moya-Len, M.A., 2007.
Treatment with 1-MCP and the role of ethylene in aroma development of mountain papaya fruit. Postharvest Biol. Technol. 43, 6777.
Belitz, H.D., Grosch, W., 1999. Food Chemistry. Springer-Verlag, Berlin, Germany.
Blankenship, S.M., Dole, J.M., 2003. 1-Methylcyclopropene: a review. Postharvest
Biol. Technol. 28, 125.
Blumenthal, R.D., Lew, W., Reising, A., Soyne, D., Osorio, L., Ying, Z., Goldenberg,
D., 2000. Antioxidant vitamins reduce normal tissue toxicity induced by radioimmunotherapy. Int. J. Cancer 86, 276280.
Chang, J.C., Lin, C.C., Wu, S.J., Lin, D.L., Wang, S.S., Miaw, C.L., Ng, L.T., 2008.
Antioxidative and hepatoprotective effects of Physalis peruviana extract against
acetaminophen-induced liver injury in rats. Pharmaceut. Biol. 46, 724731.
Davey, M.W., van Montagu, M., Inz, D., Sanmartin, M., Kanellis, A., Smirnoff, N., Benzie, I.J.J., Strain, J.J., Favell, D., Fletcher, J., 2000. Plant l-ascorbic acid: chemistry,
function, metabolism, bioavailability and effects of processing. J. Sci. Food Agric.
80, 825860.
Egea, M.I., Flores, F.B., Martinez-Madrid, M.C., Romojaro, F., Snchez-Bel, P., 2010.
1-Methylcyclopropene affects the antioxidant system of apricots (Prunus armeniaca L. cv. Bulida) during storage at low temperature. J. Sci. Food Agric. 90,
549555.

M. Valdenegro et al. / Postharvest Biology and Technology 67 (2012) 110117

Englard, S., Seifter, S., 1986. The biochemical functions of ascorbic-acid. Annu. Rev.
Nutr. 6, 365406.
Flores, F.B., Snchez-Bel, P., Valdenegro, M., Romojaro, F., Martnez-Madrid, M.C.,
Egaea, M.I., 2008. Effects of a pretreatment with nitric oxide on peach (Prunus
persica L.) storage at room temperature. Eur. Food Res. Technol. 227, 15991611.
Frankel, E., Waterhouse, A., Teissedre, P., 1995. Principal phenolic phytochemicals in
selected California wines and their antioxidant activity in inhibiting oxidation
of human low-density lipoproteins. J. Agric. Food Chem. 43, 890894.
Galati, E.M., Mondello, M.R., Giuffrida, D., Dugo, G., Miceli, N., Pergolizzi, S., Taviano,
M.F., 2003. Chemical characterization and biological effects of sicilian Opuntia
Ficus-Indica (L.) fruit juice: antioxidant and antiulcerogenic activity. J. Agric. Food
Chem. 51, 49034908.
Giugliano, D., 2000. Dietary antioxidants for cardiovascular prevention. Nutr. Metab.
Cardiovasc. Dis. 10, 3844.
Gutierrez, M.S., Trinchero, G.D., Cerri, A.M., Vilella, F., Sozzi, G.O., 2008. Different
responses of goldenberry fruit treated at four maturity stages with the ethylene
antagonist 1-methylcyclopropene. Postharvest Biol. Technol. 48, 199205.
Haegele, A.D., Gillette, C., ONeill, C., Wolfe, P., Heimedinger, J., Sedlacek, S., Thompson, H.J., 2000. Plasma xanthophyll carotenoids correlate inversely with indices
of oxidative DNA damage and lipid peroxidation. Cancer Epidemiol. Biomarkers
Prev. 9, 421425.
Hewett, E.W., 1993. New horticultural crops in New Zealand. In: Janick, J., Simon,
J.E. (Eds.), New Crops. John Wiley & Sons Inc., New York, pp. 5764.
Huang, D., Ou, B., Prior, R.L., 2005. The chemistry behind antioxidant capacity assays.
J. Agric. Food Chem. 53, 18411856.
Islas-Osuna, M.A., Stephens-Camacho, N.A., Contreras-Vergara, C.A., RiveraDominguez, M., Sanchez-Sanchez, E., Villegas-Ochoa, M.A., Gonzalez-Aguilar,
G.A., 2010. Novel postharvest treatment reduces ascorbic acid losses in mango
(Mangifera indica L.) var. Kent. Amer. J. Agric. Biol. Sci. 5, 342349.
Kinsella, J.E., Frankel, E., German, B., Kanner, J., 1993. Possible mechanism for the
protective role of antioxidants in wine and plants foods. Food Technol. 47, 8589.
Kleszczewska, E., 2000. l-Ascorbic acid clinical use, toxicity, properties, methods
of determination and application in chemical analysis. Pharmazie 55, 640644.
Majumder, K., Mazumdar, B.C., 2002. Changes of pectic substances in developing
fruits of cape-gooseberry (Physalis peruviana L.) in relation to the enzyme activity
and evolution of ethylene. Sci. Hort. 96, 91101.
Mc Cain, R., 1993. Goldenberry, passionfruit & white sapote: potential fruits for cool
subtropical areas. In: Janick, J., Simon, J.E. (Eds.), New Crops. John Wiley & Sons
Inc., New York, pp. 479486.
Miller, N.J., Rice-Evans, C.A., 1997. The relative contributions of ascorbic acid and
phenolic antioxidants to the total antioxidant activity of orange and apple fruit
juices and blackcurrant drink. Food Chem. 60, 331337.
Morton, J., 1987. Cape gooseberry. In: Morton, J.F. (Ed.), Fruits of Warm Climates.
Miami, Florida, pp. 430434.
Moya-Len, M.A., Vergara, M., Bravo, C., Montes, M.E., Moggia, C., 2006. 1-MCP treatment preserves aroma quality of Packhams Triumph pears during long-term
storage. Postharvest Biol. Technol. 42, 185197.
Murcia, M.A., Egea, M.I., Romojaro, F., Parras, P., Jimnez, A.M., Martinez-Tom, M.,
2004. Antioxidant evaluation in dessert spices compared with common food
additives. Inuence of irradiation procedure. J. Agric. Food Chem. 52, 18721881.
Murcia, M.A., Jimnez-Monreal, A.M., Garca-Diaz, L., Carmona, M., Maggi, L.,
Martnez-Tom, M., 2009. Antioxidant activity of minimally processed (in modied atmospheres), dehydrated and ready-to-eat vegetables. Food Chem. Toxicol.
47, 21032110.

117

Pavet, V., Olmos, E., Kiddle, G., Mowla, S., Kumar, S., Antoniw, J., Alvarez, M.E., Foyer,
C.H., 2005. Ascorbic acid deciency activates cell death and disease resistance
responses in Arabidopsis. Plant Physiol. 139, 12911303.
Pellegrini, N., Riso, P., Porrinni, M., 2000. Tomato consumption does not affect the
total antioxidant capacity of plasma. Nutrition 16, 268271.
Pinto, M.S., Ranilla, L.G., Apostolidis, E., Lajolo, F.M., Genovese, M.I., Shetty, K., 2009.
Evaluation of antihyperglycemia and antihypertension potential of native peruvian fruits using in vitro models. J. Med. Food 12, 278291.
Ramadan, M.F., 2011a. Bioactive phytochemicals, nutritional value, and functional
properties of cape gooseberry (Physalis peruviana): an overview. Food Res.
Intern. 44, 18301836.
Ramadan, M.F., 2011b. Physalis peruviana: a rich source of bioactive phytochemicals
for functional foods and pharmaceuticals. Food Rev. Intern. 27, 259273.
Ramadan, M.F., Mrsel, J.T., 2007. Impact of enzymatic treatment on chemical
composition, physicochemical properties and radical scavenging activity of
goldenberry (Physalis peruviana L.) juice. J. Sci. Food Agric. 87, 452460.
Ramadan, M.F., Mrsel, J.T., 2009. Oil extractability from enzymatically treated goldenberry (Physalis peruviana L.) pomace: range of operational variables. Intern. J.
Food Sci. Technol. 44, 435444.
Scheen, A.J., 2000. Antioxidant vitamins in the prevention of cardiovascular disease.
Second part: results of clinical trials. Rev. Med. Liege 55, 105109.
Trinchero, G., Sozzi, G., Cerri, A.M., Vilella, F., Fraschina, A., 1999. Ripening-related
changes in ethylene production, respiration rate and cell-wall enzyme activity
in goldenberry (Physalis peruviana L.), a solanaceous species. Postharvest Biol.
Technol. 16, 139145.
Van den Berg, R., Haenen, G.R.M.M., Van den Berg, H., Bast, A., 1999. Applicability of an improved Trolox equivalent antioxidant capacity (TEAC) assay for
evaluation of antioxidant capacity measurements of mixtures. Food Chem. 66,
511517.
Vanacker, H., Sandalio, L.M., Jimnez, A., Palma, J.M., Corpas, F.J., Meseguer, V.,
Gmez, M., Sevilla, F., Leterrier, M., Foyer, C.H., Del Ro, L.A., 2006. Roles for
redox regulation in leaf senescence of pea plants grown on different sources of
nitrogen nutrition. J. Exp. Bot. 57, 17351745.
Vinson, J.A., Su, X., Zubik, L., Bose, P., 2001. Phenol antioxidant quantity and quality
in foods: fruits. J. Agric. Food Chem. 49, 53155321.
Wang, H., Cao, G.H., Prior, R.L., 1996. Total antioxidant capacity of fruits. J. Agric.
Food Chem. 44, 701705.
Watkins, C.B., 2002. Ethylene synthesis, mode of action, consequences and control.
In: Knee, M. (Ed.), Fruit Quality and its Biological Basis. Shefeld Academic Press,
pp. 180224.
Wimalasiri, P., Wills, R.B.M., 1983. Simultaneous analysis of ascorbic and
dehydroascorbic acid in fruit and vegetables by high-performance liquid chromatography. J. Chromatogr. 256, 368371.
Wu, S.J., Ng, L.T., Huang, Y.M., Lin, D.L., Wang, S.S., Huang, S.N., Lin, C.C., 2005. Antioxidant activities of Physalis peruviana. Biol. Pharm. Bull. 28, 963966.
Wu, S.J., Ng, L.T., Lin, D.L., Wang, S.S., Lin, C.C., 2004. Physalis peruviana extract
induces apoptosis in human Hep G2 cells through CD95/CD95L system and
mitochondrial signalling transduction pathway. Cancer Lett. 215, 199208.
Wu, S.J., Tsai, J.Y., Chang, S.P., Lin, D.L., Wang, S.S., Huang, S.N., Ng, L.T., 2006.
Supercritical carbon dioxide extract exhibits enhanced antioxidant and antiinammatory activities of Physalis peruviana. J. Ethnopharmacol. 108, 407413.
Yamaguchi, T., Takamura, H., Matoba, T., Terao, J., 1998. HPLC method for evaluation
of the free radical-scavenging activity of foods by using 1,1-diphenyl-2picrylhydrazyl. Biosci. Biotechnol. Biochem. 62, 12011204.