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Postharvest Biology and Technology 139 (2018) 91–98

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Postharvest Biology and Technology


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

Cold storage temperatures and durations affect the concentrations of lupeol, T


mangiferin, phenolic acids and other health-promoting compounds in the
pulp and peel of ripe mango fruit

Mekhala Dinushi Kananke Vithanaa, Zora Singha, , Stuart K. Johnsonb
a
Curtin Horticulture Research Laboratory, School of Molecular and Life Sciences, Faculty of Science and Engineering, Curtin University, GPO Box U1987, Perth 6845,
Western Australia, Australia
b
School of Public Health, Curtin Health Innovation Research Institute, Faculty of Health Sciences, Curtin University, GPO Box U1987, Perth 6845, Western Australia,
Australia

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

Chemical compounds studied in this article: Mangoes are usually stored above 13 °C to avoid chilling injury. We investigated the effects of cold storage
Lupeol (PubChem CID: 259846) temperatures (5 and 13 °C) and durations (12 and 24 d) on the concentrations of lupeol, mangiferin, phenolic
Mangiferin (PubChem CID: 5281647) acids (gallic, chlorogenic, vanillic, ferulic and caffeic), ascorbic acid, carotenoids, total phenols and antioxidants
Gallic acid (PubChem CID: 370) in the pulp and peel of ripe ‘Kensington Pride’ mango fruit. Mature green mangoes were stored at 5 °C (chilling)
Chlorogenic acid (PubChem CID: 1794427)
or 13 °C (non-chilling) temperature for 12 and 24 d prior to ripening at ambient temperature (21 ± 1.5 °C).
Vanillic acid (PubChem CID: 8468)
Chilling injury and concentrations of health-promoting compounds were determined at eating soft ripe stage.
Ferulic acid (PubChem CID: 445858)
Caffeic acid (PubChem CID: 689043) Chilling injury symptoms were only developed on ripe fruit following storage at 5 °C for 24 d. The concentrations
Ascorbic acid (PubChem CID: 54670067) of lupeol in pulp and peel, chlorogenic and caffeic acids in the pulp were significantly higher in fruit stored at
5 °C than 13 °C, whilst mangiferin, gallic, chlorogenic, vanillic, ferulic, and caffeic acids, total phenols, anti-
Keywords:
Mango oxidants and carotenoids in the peel were significantly higher when stored at 13 °C. The concentrations of lupeol
Low-temperature storage and chlorogenic acid in pulp and peel and gallic acid in the pulp were significantly lower when stored for 24 d
Chilling injury compared to 12 d, whilst vanillic acid, total phenols, total antioxidants and ascorbic acid in the pulp and caffeic
Health-promoting compounds acid in both pulp and peel were significantly higher when stored for 24 d. In conclusion, cold storage tem-
Lupeol peratures and duration influence the concentration of lupeol, mangiferin, phenolic acids and other health-
Mangiferin promoting compounds in the pulp and peel of ripe mango fruit. Storage of mature green mangoes at chilling
Phenolic acids temperature (5 °C) for 12 d prior to ripening (21 ± 1.5 °C) seems to be a promising tool for maximizing the
levels of lupeol in the pulp and peel of the fruit.

1. Introduction anticancer, antimicrobial, cardio-protective and anti-inflammatory


(Masibo and He, 2008). Moreover, a number of studies have revealed
Mango (Mangifera indica L.) is globally known for its appealing taste that the pulp, peel, seed and other parts of mango tree are good sources
and excellent nutritional quality. Additionally, particular health-pro- of health-promoting compounds including gallic acid, chlorogenic acid,
moting compounds present in this fruit are also known for their ability vanillic acid among many other polyphenolic antioxidants which have a
to reduce the risk of chronic health issues (Masibo and He, 2008). Lu- well-known potential in reducing the risk of cancer and cardiovascular
peol and mangiferin are two such compounds with a significant pro- diseases (Ajila et al., 2007; Masibo and He, 2008; Kim et al., 2010).
tective potential. Lupeol, a triterpene is one of the most important anti- Mango fruit is also rich in other dietary antioxidants, such as ascorbic
carcinogenic compounds present in mango, and has been found to be acid and carotenoids which contribute to its health promoting potential
capable of reducing the risk of a number of serious human diseases (Kim et al., 2007; Ma et al., 2011).
including cancer, cardiovascular diseases, diabetes, liver toxicity and The storage life of mango fruit is extremely limited; with fruit
renal diseases (Saleem, 2009; Siddique and Saleem, 2011 Siddique and usually ripen in a week after harvest at mature green stage at ambient
Saleem, 2011). Mangiferin, a glucosyl xanthone is also known for its temperature (Singh et al., 2013). Therefore; the mango fruit are usually
wide range of health protective properties such as antioxidant, stored under low temperatures to prolong storage life (Chaplin et al.,


Corresponding author.
E-mail address: Z.Singh@curtin.edu.au (Z. Singh).

https://doi.org/10.1016/j.postharvbio.2017.12.003
Received 21 October 2017; Received in revised form 3 December 2017; Accepted 12 December 2017
0925-5214/ © 2018 Elsevier B.V. All rights reserved.
M.D.K. Vithana et al. Postharvest Biology and Technology 139 (2018) 91–98

1991; Medlicott et al., 1990; Talcott et al., 2005). Cold storage tech- The fruit stored at standard low temperature storage (13 °C) for 12 and
nology; however, cannot be exploited to its full potential in extending 24 days reached the eating soft stage in 4 and 5 days respectively. The
storage life of tropical and subtropical fruit including mango because of experiment followed two-factor factorial design (storage temperature
their susceptibility to chilling injury. Mango fruit when stored below and storage duration). Ten mangoes were used for each treatment unit
13 °C develop chilling injury symptoms (Chaplin et al., 1991). Pre- and replicated four times.
viously, the impact of low-temperature storage on chilling injury and Once mangoes reached the eating soft stage, the chilling injury
physico-chemical parameters such as colour, pulp firmness, soluble symptoms were recorded. The peel and pulp samples (cut in to small
solids concentration, acidity and total and individual sugars of mango pieces) of 10 mango fruit in each replication were immediately stored
fruit have been reported (Chaplin et al., 1991; Nair and Singh, 2009; at −80 °C for the later determination of lupeol, mangiferin, phenolic
Robles-Sánchez et al., 2009; Sankat et al., 1994). Some limited and acids, total phenols, total antioxidants, ascorbic acid and total car-
inconclusive research has been reported on the impact of cold storage otenoids. The concentrations of total phenols, total antioxidants, as-
and chilling injury on the concentrations of health-promoting com- corbic acid and total carotenoids were determined using thawed sam-
pounds such as ascorbic acid, total antioxidants, total carotenoids and ples of each replication. Some representative frozen, samples were
total phenols in mango fruit (Kondo et al., 2005; Nair and Singh., 2009; freeze dried at −50 °C and 1 × 10−1 mB vacuum pressure (Telstar
Robles-Sánchez et al., 2009). However, no research work has been re- Cryodos V 1.0, Terrassa, Spain), powdered and stored at − 20 °C for the
ported on the effects of low temperature storage on the concentrations later determination of the concentrations of lupeol, mangiferin and
of potential anticancer compounds such as lupeol, mangiferin and phenolic acids.
phenolic acids including gallic acid, chlorogenic acid and vanillic acid
in the pulp and peel of mango fruit. 2.1.2. Chemicals
Given the potential health benefits of polyphenols, there have been All reagents and standards of lupeol, mangiferin, phenolic acids, β-
recent reports in the use of physical elicitors (low temperature storage, carotene, L-ascorbic acid and Trolox were purchased from Sigma
heat treatment, controlled and modified atmosphere storage) and che- Aldrich (St. Louis, MO, USA) whilst methanol, acetonitrile and n-
mical elicitors (methyl jasmonate, salicylic acid and ethylene) as an hexane were purchased from Thermo Fisher Scientific (Thermo Fisher
effective tool to trigger their production in fruit and vegetables (Ruiz- Scientific, Taren Point, NSW, Australia). Only HPLC grade reagents and
Garcia and Gomez-Plaza, 2013; Schreiner and Huyskens-Keil, 2006). standards were used in the study.
The low temperature stress is believed to induce the biosynthesis of
polyphenols via the shikimic acid pathway as a part of the plant defence 2.2. Chilling injury (CI)
mechanism (Ruiz-Garcia and Gomez-Plaza, 2013). Previously, Rivera-
Pastrana et al. (2010) claimed an increased level of total antioxidants The level of chilling injury (CI) on the ripe mango fruit was recorded
and better retention of ferulic acid and caffeic acid in the chill-sensitive using the following rating scale previously described by Zaharah and
fruit papaya; when stored at 5 °C. Therefore, the effect of cold storage Singh (2011); 0- no damage, 1- very light damage (< 5% of the surface
temperatures and periods on the levels of phenolic compounds in ripe damaged), 2- light damage (5–10% of the surface is damaged), 3-
mango fruit warrants to be investigated as a potential tool to enhance moderate damage (11–24%) and 4- severe damage (25–50% of the
its health beneficial properties. surface damaged). The chilling injury index was calculated using the
In this study, it was hypothesised that the chill-storage temperature following formula;
would increase the concentrations of lupeol, mangiferin and phenolic
Σ(Injury level × number of fruit at each level)
acids (chlorogenic acid, gallic acid, vanillic acid, ferulic acid and caffeic
Total number of fruit
acid) and other health-promoting compounds (ascorbic acid and car-
otenoids) as a response to low temperature stress. To the best of our
knowledge this is the first study on the effect of chilling and non-chil- 2.3. Determination of the concentrations of health-promoting compounds
ling low temperature storage and period on the concentrations of lu-
peol, mangiferin and phenolic acids (gallic acid, chlorogenic acid, va- 2.3.1. Lupeol
nillic acid, ferulic acid and caffeic acid) in ripe mango fruit. Lupeol was extracted from the freeze dried mango pulp/peel and
quantified using an Agilent HPLC system (1200 series, Agilent
2. Materials and methods Technologies, Ratingen, Germany) fixed with a diode array detector
(1200 Infinity, Agilent Technologies). The method was developed based
2.1. Materials on the previous reports of Ruiz-Montañez et al. (2014) and Oliveira
et al. (2012) with some modifications detailed in our previous paper
2.1.1. Fruit (Vithana et al., 2017). The amount of lupeol was quantified using a
Hard green mature ‘Kensington Pride’ mango fruit (light cream standard curve and expressed as mg kg−1 dry weight basis.
pulp, firmness: 165 ± 1 N) were harvested from a commercial orchard
in Gingin (31° 27′S, 115° 55′E), Western Australia and transported 2.3.2. Total phenols
within 2 h to the laboratory on the 9th of March 2015. Only mango fruit The total phenol concentration was estimated following the method
free from visual symptoms of mechanical, chemical or insect-pest in- described earlier by Robles-Sánchez et al. (2009) using Folin-Ciocalteu
juries and symptoms of disease(s) were used in the study. The selected reagent with slight modifications which have been described in our
fruit were treated with the fungicide (Sportak (0.55 ml L−1) containing previous paper (Vithana et al., 2017). A UV/VIS spectrophotometer
prochloraz as the active ingredient (Bayer CropScience Pty Ltd., (Jenway spectrophotometer Model 6405, Dunmow, Essesx, UK) was
Victoria, Australia) and allowed to dry. The fruit were packed into used to record the absorbance at 750 nm. A gallic acid standard curve
cardboard boxes and stored at either 5 °C or 13 °C at 85% ± 0.5% re- was used to calculate the total phenol concentration and the values
lative humidity in dark for either 12 d or 24 d. After each storage period were expressed in g GAE kg−1 fresh weight basis.
at both temperatures, the fruit were allowed to ripen at ambient tem-
perature (21 ± 1.5 °C) until eating soft stage (depending upon peel and 2.3.3. Mangiferin and phenolic acids
pulp yellow colour > 75% and/or firmness: 7.0–9.0 N). The number of Determination of the concentrations of mangiferin and phenolic
days taken for the fruit to reach the eating soft stage differed depending acids (gallic, chlorogenic, vanillic, ferulic and caffeic) was carried out
upon the treatment (Fig. 1). Six and nine days were taken to reach this following the method previously described by Palafox-Carlos et al.
stage by the fruit stored at 5 °C for 12 d and 5 °C for 24 d respectively. (2012) using Agilent HPLC system (Agilent Technologies) equipped

92
M.D.K. Vithana et al. Postharvest Biology and Technology 139 (2018) 91–98

Fig. 1. The mango fruit at eating soft stage following the cold storage at different temperature. (A) – Fruit stored at 5 °C for 12 d, (B) – Fruit stored at 5 °C for 24 d, (C) – Fruit stored at
13 °C for 12 d, (D) – Fruit stored at 13 °C for 24 d.

with a diode array detector (DAD) (Agilent Technologies) with few storage temperature, storage duration and their interaction on chilling
modifications and conditions of analysis that have been previously re- injury and the concentrations of health-promoting compounds were
ported in our joint paper (Vithana et al., 2017). The concentrations of assessed. Genstat version 14.0 (Lawes Agricultural Trust, Rothamsted,
polyphenols were quantified using standard curves of each compound UK) software was used to analyze the data.
and expressed as mg kg−1 dry weight basis.

2.3.4. Ascorbic acid 3. Results


The method described previously by Malik and Singh (2005) and in
our recent paper (Vithana et al., 2017) was followed to determine the 3.1. Chilling injury (CI)
concentration of ascorbic acid in the fruit pulp. The absorbance at
760 nm was recorded using a UV/vis spectrophotometer (Jenway) and Chilling injury symptoms were only developed in those mangoes
the amount of ascorbic acid was calculated based on an L-ascorbic acid stored at 5 °C for 24 d after ripening at room temperature
standard curve and expressed as mg kg−1 fresh weight basis. (21 ± 1.5 °C). The CI index was the highest (1.8) when the fruit were
stored at 5 °C for 24 d following ripening at room temperature
2.3.5. Total carotenoids (21 ± 1.5 °C) for 7 d when compared to all other treatments (0)
The method earlier described by Lalel et al. (2003) was used to (Fig. 2).
determine the concentration of total carotenoids in the pulp of ripe
mango fruit. The absorbance at 436 nm was recorded using a UV/VIS
spectrophotometer (Jenway) and the concentration of total carotenoids
was calculated using a β- carotene standard curve and expressed as
mg kg−1 fresh weight basis.

2.3.6. Total antioxidants


The DPPH (2, 2-diphenyl-1-picrylhydrazyl) assay described by
Brand-Williams et al. (1995) was used to assess the total antioxidant
capacity in the pulp and peel of ripe mango fruit. The absorbance was
measured at 515 nm and the total antioxidant capacity was estimated
using a standard curve of Trolox. Results were expressed as mmol
Trolox equivalent antioxidant capacity (TEAC) kg−1 fresh weight basis.

2.4. Statistical analysis

Data were subjected to two-way ANOVA (low storage temperatures Fig. 2. Chilling injury index of the ripe mango fruit following cold storage at 5 °C and
and storage duration). Least significant differences were calculated 13 °C for 12 d or 24 d. n = 4, 10 fruit in each replicate. The vertical bar shows the
standard deviation of means.
using Fisher’s Protected Least Significant Test (P ≤ 0.05). The effect of

93
M.D.K. Vithana et al. Postharvest Biology and Technology 139 (2018) 91–98

DW = Dry weight, ST = Storage temperature, SP = Storage period, ST × SP = Storage temperature × storage period interaction, NS = Not significant, n = 4 ± SD, 10 fruit per replication. Mean values significantly different at P ≤ 0.05 are
indicated by lower case, superscript letters within the comparison between storage temperature and period. Significant difference between the mean storage temperatures with each period is represented by different upper case, superscript letters.
3.2. Effect of chilling and non-chilling storage temperatures and durations

Mean (ST)

ST × SP
on concentration of health-promoting compounds

1.023
11.9A
10.9B
3.2.1. Lupeol and mangiferin
The concentration of lupeol in the pulp and peel of ripe mangoes

12.5 ± 0.4c
10.0 ± 0.3
was significantly affected by low storage temperature and duration
(Table 1).When averaged over both storage periods, mean concentra-

11.2
tions of lupeol were significantly higher in those fruit previously stored

NS
24

SP
at 5 °C than those previously stored at 13 °C. When averaged over both
Storage Period (d)

storage temperatures, the mean concentrations of lupeol in both pulp


bc

and peel of ripe fruit were significantly higher in 12 d stored fruit, than
11.3 ± 0.7b
11.9 ± 0.6

those stored for 24 d. Overall, the concentration of lupeol in the peel of


0.723

ripe mango fruit was 1.4 fold higher than in the pulp. The interaction
11.6
Peel

12

ST

between the low storage temperature and duration was significant


(P ≤ 0.05) for the concentrations of lupeol in both the pulp and peel.
The storage duration did not significantly affect the concentration of
Mean (ST)

ST × SP

mangiferin in the pulp and peel of ripe fruit (Table 1). Its concentration
2.141
10.6

in the pulp of ripe fruit was not affected by the storage temperature
9.0

whilst, in the peel it was significantly (P ≤ 0.05) lower in the fruit


previously kept at 5 °C compared to those kept at 13 °C. The interaction
a

8.9 ± 0.1a

between low storage temperature and duration was significant for the
9.2 ± 0.2
Mangiferin (mg kg−1 DW)

concentrations of mangiferin in both the pulp and peel. The pulp of the
ripe mango fruit previously stored at 13 °C for 12 d and peel of those
9.1

NS
24

SP

fruit stored at 13 °C for 24 d exhibited the highest concentrations of


Storage period (d)

mangiferin (Table 1). Across all samples, the concentration of mangi-


12.2 ± 2.3b

ferin in the peel of ripe mango fruit on average was 1.2 times higher
a
8.8 ± 0.1

than pulp.
The concentrations of lupeol and mangiferin in the pulp and peel of ripe mangoes exposed to different cold storage temperatures and durations.

Pulp

10.5

NS
12

ST

3.2.2. Phenolic acids


Gallic, chlorogenic, vanillic, ferulic and caffeic acids were identified
Mean (ST)

in the pulp and peel of all ripe mangoes previously stored at chilling
ST × SP

(5 °C) and non-chilling (13 °C) temperatures for 12 or 24 d (Table 2).


2.041
A
14.9
9.7B

Their concentrations in both pulp and peel were significantly affected


(P ≤ 0.05) by the low storage temperature except for the concentration
of ferulic acid in pulp. The storage duration also influenced the con-
b
14.5 ± 1.2
4.1 ± 0.1a

centrations of all of the phenolic acids in the pulp except that of ferulic
acid. The concentrations of gallic, vanillic and ferulic acids in the peel
1.443
9.3B

were also not significantly (P ≤ 0.05) affected by the storage duration.


24

SP

The interaction between low storage temperature and duration was


Storage Period (d)

found to be significant (P ≤ 0.05) for the concentrations of gallic, va-


b

15.3 ± 1.2b
15.2 ± 1.1

nillic, ferulic and caffeic acids in the peel and the concentration of
vanillic and caffeic acids in the pulp. When averaged over both storage
1.443
15.3A
Peel

periods, mean concentrations of gallic acid and vanillic acid in both


12

ST

pulp and peel and the concentrations of chlorogenic, ferulic and caffeic
acids in peel of ripe fruit were significantly higher when stored at 13 °C
All of the lettering is separate for pulp and peel and for different compounds.
Mean (ST)

compared to 5 °C (Table 2). When averaged over storage temperatures,


ST × SP

the mean concentrations of gallic acid and chlorogenic acid in the pulp
1.535
A
10.4
7.2B

and the concentration of chlorogenic acid in peel were significantly


higher in 12 d cold stored fruit than those stored for 24 d. In contrast,
the concentrations of vanillic and caffeic acids in the pulp of ripe fruit
b

3.7 ± 0.2a
8.4 ± 1.0

were significantly higher after 24 d of cold storage, irrespective of the


1.086

storage temperature (Table 2). Overall, the concentrations of gallic


6.0B
Lupeol (mg kg−1 DW)

24

SP

acid, chlorogenic acid, vanillic acid, ferulic acid and caffeic acids in the
Storage period (d)

peel of ripe mango fruit were 2.6, 1.6, 2.6, 2.6 and 16.0 times higher
respectively than in the pulp.
d

10.8 ± 0.7c
12.3 ± 1.3

3.2.3. Total phenols and total antioxidant capacity


1.086
11.6A
Pulp

12

The concentration of total phenols in the pulp was significantly


ST

affected only by the low temperature storage period (P ≤ 0.05). The


mean concentration of total phenols in the pulp was significantly higher
Storage temperature

when stored for 24 d than in those stored for 12 d, irrespective of the


LSD (P ≤ 0.05)

storage temperature (Table 3). Whilst, the mean concentration of total


phenols in the peel was significantly higher in the fruit previously
Mean (SP)

stored at 13 °C than those stored at 5 °C.


Table 1

13 °C
5 °C

When averaged over the storage period, the mean total antioxidant
capacity in the pulp was significantly higher in those fruit stored at 5 °C

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M.D.K. Vithana et al. Postharvest Biology and Technology 139 (2018) 91–98

Table 2
The concentrations of phenolic acids: gallic, vanillic, caffeic, chlorogenic and ferulic in the pulp and peel of ripe mangoes exposed to different cold storage temperatures and durations.

Storage temperature Pulp Peel


Storage period (d) Storage period (d)

12 24 Mean (ST) 12 24 Mean (ST)

−1
Gallic acid (mg kg DW)
5 °C 213.0 ± 9.9bc 75.0 ± 10.2a 144.0B 213.3 ± 11.9a 207.0 ± 48.2a 210.0B
13 °C 290.0 ± 77.2c 140.0 ± 16.7a 215.0A
654.0 ± 44.3c 793.0 ± 90.5b 723.5A
Mean (SP) 252.0A 107.5B 434.0 500.0
LSD (P ≤ 0.05) ST SP ST × SP ST SP ST × SP
55.8 55.8 NS 70.9 NS 100.3

Vanillic acid (mg kg−1 DW)


5 °C 77.4 ± 7.2a 81.9 ± 7.9a 79.7B 198.233.7b 106.7 ± 7.6a 152.5B
13 °C 79.9 ± 5.1a 124.9 ± 7.3b 102.4A 280.7 ± 49.9c 374.9 ± 37.4d 327.8A
Mean (SP) 78.9B 103.4A 239.4 240.8
LSD (P ≤ 0.05) ST SP ST × SP ST SP ST × SP
10.3 10.3 14.5 40.1 NS 56.7

Caffeic acid (mg kg−1 DW)


5 °C 1.7 ± 0.1b 2.9 ± 0.3c 2.3A 19.6 ± 2.3a 25.8 ± 4.7a 22.7B
13 °C 1.1 ± 0.4a 2.2 ± 0.5b 1.65B 33.7 ± 7.2a 46.9 ± 11.1b 40.3A
Mean (SP) 1.4B 2.55A 26.7B 36.4A
LSD (P ≤ 0.05) ST SP ST × SP ST SP ST × SP
0.5 0.5 0.7 7.8 7.8 11.03

Chlorogenic acid (mg kg−1 DW)


5 °C 174.4 ± 42.3 129.7 ± 8.2 152.1A 242.4 ± 21.6 121.8 ± 16.1 182.1B
13 °C 128.0 ± 7.1 108.2 ± 4.9 118.1B 282.0 ± 19.6 210.3 ± 63.4 246.2A
Mean (SP) 151.2A 119.9B 262.2A 166.1B
LSD (P ≤ 0.05) ST SP ST × SP ST SP ST × SP
27.9 27.9 NS 49.7 49.7 NS

Ferulic acid (mg kg−1 DW)


5 °C 16.0 ± 1.8 17.8 ± 4.5 16.9 35.8 ± 7.4a 28.3 ± 3.8a 32.05B
13 °C 21.9 ± 5.8 19.3 ± 4.0 20.6 59.3 ± 6.5b 69.2 ± 12.2b 64.25A
Mean (SP) 18.95 18.6 47.55 48.75
LSD (P ≤ 0.05) ST SP ST × SP ST SP ST × SP
NS NS NS 9.2 NS 13.03

DW = Dry weight, ST = Storage temperature, SP = Storage period, ST × SP = Storage temperature × storage period interaction, NS = Not significant, n = 4 ± SD, 10 fruit per re-
plication. Mean values significantly different at P ≤ 0.05 are indicated by lower case, superscript letters within the comparison between storage temperature and period. Significant
difference between the mean storage temperatures with each period is represented by different upper case, superscript letters. All of the lettering is separate for pulp and peel and for
different compounds.

than those kept at 13 °C. However, the trend was reversed in the peel Earlier, Nair et al. (2003) also reported similar symptoms and severity
(Table 3). The mean total antioxidant capacity in the peel was sig- of chilling injury on ‘Kensington Pride’ mango fruit when stored at 5 °C
nificantly higher in 24 d storage than 12 d storage, irrespective of the for 20 d.
storage temperature. Overall the total phenol concentration and total This study revealed that, the storage of mango fruit at 5 °C prior to
antioxidant capacity in the peel of ripe mango fruit were 22.1 and 9.7 ripening could significantly increase the concentration of lupeol in both
times higher respectively than pulp. pulp and peel at ripe stage (Table 1). On the other hand, storage at 13 °C
prior to ripening could significantly increase the concentrations of
3.2.4. Ascorbic acid and total carotenoids mangiferin (Table 1), chlorogenic acid, ferulic acid and caffeic acid in
The concentration of ascorbic acid in the pulp of ripe fruit was not the peel (Table 2) and gallic and vanillic acids in both pulp and peel of
affected by the storage temperature (P ≤ 0.05) (Table 4); however, the ripe mango fruit.
effect of cold storage duration and the interaction between storage Recently, exposure of fruit and vegetables to low temperature stress
temperature and duration were found to be significant (P ≤ 0.05). Its during storage has been identified as a treatment for triggering the
concentration in the pulp was significantly higher at 24 d cold storage production of desirable dietary phyto-chemicals with significant health
compared to 12 d, irrespective of the storage temperature (Table 4). benefits (Schreiner and Huyskens-Keil, 2006). The biosynthetic path-
The concentration of total carotenoids in the pulp was significantly ways of terpenes and phenols are activated after an elicitor treatment
influenced only by the storage temperature (P ≤ 0.05) (Table 4). When by inducing the activity of the enzyme, phenylalanine ammonia lyase
averaged over storage periods, the mean concentration of total car- (PAL) (Cisneros-Zevallos, 2003; Ruiz-García and Gómez-Plaza, 2013).
otenoids in the pulp of ripe fruit was significantly higher when stored at Possibly, the enhanced activity of enzyme PAL may have contributed to
13 °C than in the fruit previously stored at 5 °C. the increase in the concentrations of lupeol, mangiferin and phenolic
acids seen in the present study. Similarly, Rivera-Pastrana et al. (2010)
4. Discussion reported that the concentrations of both ferulic and caffeic acids were
better retained or even increased under low-temperature storage (5 °C)
Browning of the skin, poor colour development, prominent lenticels in ‘Maradol’ papaya fruit compared to those stored at 25 °C.
and uneven ripening were the symptoms of chilling injury observed in In our study, low temperature storage for 24 d at 5 °C or 13 °C ap-
the ripe fruit which were stored at 5 °C for 24 d. However, none of these parently induces the production and/or retention of vanillic and caffeic
symptoms appeared in ripe fruit subjected to any other treatment. acids compared to 12 d (Table 2). In contrast, storage for 24 d at

95
M.D.K. Vithana et al. Postharvest Biology and Technology 139 (2018) 91–98

FW = Fresh weight, ST = Storage temperature, SP = Storage period, ST × SP = Storage temperature × storage period interaction, NS = Not significant, n = 4 ± SD, 10 fruit per replication. Mean values significantly different at P ≤ 0.05 are
indicated by lower case, superscript letters within the comparison between storage temperature and period. Significant difference between the mean storage temperatures with each period is represented by different upper case, superscript letters.
chilling (5 °C) and non-chilling (13 °C) low temperatures gave lower

Mean (ST)

ST × SP
retention of gallic and chlorogenic acids in pulp compared to 12 d

167.8A
119.6B

9.01
(Table 2). Previously, Nair and Singh (2009) reported that rate of re-
spiration in ‘Kensington Pride’ mango fruit was significantly reduced
when stored at 5 °C when compared to 15 °C and 20 °C. It is known that

206.7 ± 6.9d
c
137.9 ± 2.8
the polyphenol biosynthesis is triggered during ripening to help shield
the oxidative stress at respiratory climax (Masibo and He, 2008). Thus,

172.3B
the suppression of the rate of respiration during low temperature sto-

6.37
24

SP
rage could possibly have led to the lower production of some phenolic
Storage period (d)

acids in fruit stored at chilling temperatures (5 °C) and/or for 24 d.


Thus, the final concentration of phytochemicals could be a result of a
129.0 ± 8.5b
a
101.3 ± 2.3

balance between the activation of secondary metabolite biosynthesis as


115.1A

a defense mechanism and the respiratory demand to shield the oxida-


6.37
Peel

tive stress during respiratory climax.


12

ST

The current study showed that the effect of storage temperature was
Total antioxidant capacity (mmol TEAC kg−1 FW)

not significant on the concentration of total phenols in the pulp of ripe


Mean (ST)

‘Kensington Pride’ mango fruit (Table 3). Heredia and Cisneros-Zevallos


ST × SP
A

11.8B

(2009) also observed non-significant influence of elicitor treatments on


17.9

2.75

the concentration of total phenols in some of the fruit and vegetables


they investigated. They suggest that this apparently non responsive
b

11.5 ± 1.5a

behaviour of some fresh produce to abiotic stress might be due to si-


17.9 ± 1.8
The concentrations of total phenols and total antioxidant capacity of the pulp and peel of ripe mangoes exposed to different cold storage temperatures and durations.

milar kinetics of phenolic synthesis and degradation which balances out


14.7A

the final concentration. On the other hand, there can be a preferential


NS
24

SP

diversion of soluble phenolics to insoluble forms such as lignin and


Storage period (d)

suberin as a part of a defence response to help strengthen the cell walls


of plant tissues (Reyes et al., 2007). This mechanism possibly has oc-
b

12.2 ± 0.7a
17.9 ± 1.6

curred in the present study. The changes in the concentration of total


15.0A

phenols after elicitor application are known to be tissue dependent


Pulp

1.95
12

ST

(Reyes et al., 2007). Thus, a significantly higher mean concentration of


total phenols in the peel of ripe mango fruit previously stored at 13 °C
compared to 5 °C (Table 3) may be ascribed to the release of free
Mean (ST)

ST × SP

phenolic acids by the degradation of bound phenolic acids.


141.6A
B
103.9

27.0

The mean total antioxidant capacity of the fruit pulp was sig-
nificantly higher in fruit stored at 5 °C than at 13 °C (Table 3). The
opposite effect of storage temperature on total antioxidant capacity was
166.2 ± 17.9c
a

found in the peel (Table 3). This effect in the peel is most likely related
89.6 ± 30.0

to the higher concentration of total phenols at 13 °C (Table 3). Pre-


127.9A

viously, Reyes et al. (2007) identified a similar trend of changes in the


NS
24

SP

concentration of total phenols and the total antioxidant capacity in


sixteen fruit and vegetables, finding a significantly positive correlation
Storage period (d)

between the total phenol content and the antioxidant potential.


b

117.0 ± 18.4b
118.2 ± 16.7

The concentration of ascorbic acid in the ripe pulp of ‘Kensington


Pride’ mango fruit was not significantly influenced by the storage
117.6A

temperature (Table 4). However, it increased with extended storage


19.1
Peel

12

ST

time. Similarly, Thomas and Janave (1975) reported a net increase in


All of the lettering is separate for pulp and peel and for different compounds.

the concentration of ascorbic acid in cold stored (7 °C) ‘Alphonso’


mangoes for 16–43 d compared to the fruit kept at tropical ambient
Mean (ST)

ST × SP

temperature (28–32 °C).


A significantly lower level of total carotenoids in the pulp of ripe
5.5
5.6

NS

fruit was found at 5 °C, but no effect of storage duration was observed
Total phenols (g GAE kg−1 FW)

(Table 4). Similarly, a significant reduction in carotenoid formation was


7.0 ± 1.2
6.2 ± 1.5

noted in ripe ‘Alphonso’ mango fruit stored at 7 °C for 16–43 d com-


pared to 28–32 °C (Thomas and Janave, 1975). Vazquez-Salinas and
6.6A

1.5
24

SP
Storage period (d)

Lakshminarayana (1985) also reported a significantly higher con-


centration of carotenoids in ‘Keitt’, ‘Haden’, ‘Irwin’ and ‘Kent’ mango
4.0 ± 0.5
5.0 ± 1.1

fruit stored at 22–28 °C compared to those stored at 16–20 °C for 2–10


d. According to Saltveit (1999), the maximal carotenoid level during
Pulp

4.5B

ripening period of climacteric fruit coincides with respiration and


NS
12

ST

ethylene climaxes. As mentioned earlier, Nair and Singh (2009) re-


ported significantly lower rates of ethylene production and respiration
Storage temperature

in the ‘Kensington Pride’ mango fruit stored at 5 °C for 20 d prior to


LSD (P ≤ 0.05)

ripening. Therefore; the lower levels of total carotenoids at chilling


storage temperature (5 °C) may have been associated with the reduced
Mean (SP)

rates of respiration and ethylene production.


Table 3

13 °C
5 °C

In general it has been reported that the peel of mango fruit has
higher levels of dietary polyphenols and lupeol than pulp (Berardini

96
M.D.K. Vithana et al. Postharvest Biology and Technology 139 (2018) 91–98

Table 4
The concentrations of ascorbic acid and total carotenoids in the pulp of ripe mangoes exposed to different cold storage temperatures and durations.

Storage temperature Ascorbic acid (mg kg−1 FW) Total carotenoids (mg kg−1 FW)
Storage period (d) Storage period (d)

12 24 Mean (ST) 12 24 Mean (ST)

a b A
5 °C 329.0 ± 17.11 378.0 ± 25.7 353.5 19.5 ± 1.1 21.1 ± 0.5 20.3B
13 °C 332.0 ± 12.6a 358.0 ± 25.4b 345.0A 25.8 ± 2.6 23.2 ± 1.4 24.5A
Mean (SP) 330.5B 368.0A 22.65A 22.15A
LSD (P ≤ 0.05) ST SP ST × SP ST SP ST × SP
NS 17.35 24.54 2.03 NS NS

FW = Fresh weight, ST = Storage temperature, SP = Storage period, ST × SP = Storage temperature × storage period interaction, NS = Not significant, n = 4 ± SD, 10 fruit per
replication. Mean values significantly different at P ≤ 0.05 are indicated by lower case, superscript letters within the comparison between storage temperature and period. Significant
difference between the mean storage temperatures with each period is represented by different upper case, superscript letters. All of the lettering is separate for pulp and peel and for
different compounds.

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at either chill or standard low temperature may also provide a good fruit by HPLC–DAD–MS/MS-ESI and their individual contribution to the antioxidant
activity during ripening. Food Chem. 135 (1), 105–111.
source of health-promoting compounds for food processing and nu- Reyes, L.F., Villarreal, J.E., Cisneros-Zevallos, L., 2007. The increase in antioxidant ca-
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Rivera-Pastrana, D.M., Yahia, E.M., González-Aguilar, G.A., 2010. Phenolic and car-
Acknowledgements otenoid profiles of papaya fruit (Carica papaya L.) and their contents under low
temperature storage. J. Sci. Food Agric. 90 (14), 2358–2365.
M.D.K Vithana is thankful for Endeavour Postgraduate Award (PhD) Robles-Sánchez, R.M., Islas-Osuna, M.A., Astiazarán-García, H., Vázquez-Ortiz, F.A.,
Martín-Belloso, O., Gorinstein, S., González-Aguilar, G.A., 2009. Quality index,
offered by the Australian Government and Wayamba University of Sri consumer acceptability, bioactive compounds, and antioxidant activity of fresh-cut
Lanka for granting study leave during her PhD. Mr. Edwin Junaldi and Ataulfo mangoes (Mangifera indica L.) as affected by low-temperature Storage. J.
Ms. Susan Petersen are gratefully acknowledged for the technical sup- Food Sci. 74 (3), S126–S134.
Ruiz-García, Y., Gómez-Plaza, E., 2013. Elicitors: a tool for improving fruit phenolic
port provided in determination of polyphenolic profile and lupeol using content. Agriculture 3 (1), 33–52.
HPLC-diode array detection. Ruiz-Montañez, G., Ragazzo-Sánchez, J.A., Calderón-Santoyo, M., Velazquez-De La Cruz,
G., de León, J.R., Navarro-Ocaña, A., 2014. Evaluation of extraction methods for
preparative scale obtention of mangiferin and lupeol from mango peels (Mangifera
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