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Effect of ammonium content in nutrition solution on vitamin C, phenols, and antioxidant capacity of three apple cultivars during cold storage

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Pre-harvest nutritional condition is one of the major fruit quality influencers in apple whether directly after harvest or throughout cold storage. Here, the influences of various levels of ammonium to nitrate on vitamin C content, total phenolic compounds, and total antioxidant capacity of three apple cultivars ('Granny Smith', 'Gala', and 'Golab Kohans') throughout cold storage period were studied. Five different ammonium nitrogen levels (0, 0.08, 0.16, 0.19, and 0.27 meq/L) were applied. After harvest, the fruits were transferred to cold storage and stored at 0±1˚C for 45, 90, and 160 days for 'Golab Kohans', 'Gala', and 'Granny Smith', respectively. Vitamin C content, total phenolic compounds, and total antioxidant capacity were determined throughout the storage period. The results showed that all cultivars showed different responses toward ammonium nitrogen application in terms of vitamin C content. 'Golab Kohans' recorded an increase in vitamin C content by increasing ammonium in nutrition solutions. On the other hand, minor changes were recorded in 'Granny Smith' and 'Gala'. Total phenolic compounds and total antioxidant capacity were significantly increased under all tested levels of ammonium in comparison to control in all cultivars. Furthermore, all cultivars showed a significant decrease in vitamin C, total phenolic compounds, and total antioxidant capacity throughout cold storage, indicating that these bioactive compounds were subjected to decomposition and metabolic degradation during the storage period. Surface response analysis results showed that more vitamin C degradation was attributed to the increase in ammonium application, while less total phenolic compounds degradation and total antioxidant capacity decrease were observed under similar treatments.
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E-NAMTILA Publishing DYSONA - Applied Science
DAS 1 (2020) 64-72 DOI: 10.30493/DAS.2020.230629
64
All published articles in DYSONA - Applied Science
journal are distributed under a Creative Commons Attribution 4.0
International License.
DYSONA Applied Science ISSN: 2708-6283
Effect of ammonium content in nutrition
solution on vitamin C, phenols, and
antioxidant capacity of three apple cultivars
during cold storage
Fares Alhaj Alali1; Mohammad Ali Askari Sarcheshmeh1*; Mesbah Babalar1
1, Department of Horticultural Sciences, College of Agriculture and Natural Resources (UTCAN), University of Tehran, Karaj, Iran
Abstract
E-mail:
askari@ut.ac.ir
Received: 10/05/2020
Acceptance: 26/06/2020
Available Online: 27/06/2020
Published: 01/07/2020
Pre-harvest nutritional condition is one of the major fruit quality influencers in
apple whether directly after harvest or throughout cold storage. Here, the
influences of various levels of ammonium to nitrate on vitamin C content, total
phenolic compounds, and total antioxidant capacity of three apple cultivars
(‘Granny Smith’, ‘Gala’, and ‘Golab Kohans’) throughout cold storage period
were studied. Five different ammonium nitrogen levels (0, 0.08, 0.16, 0.19, and
0.27 meq/L) were applied. After harvest, the fruits were transferred to cold
storage and stored at 0±1˚C for 45, 90, and 160 days for ‘Golab Kohans’, Gala’,
and ‘Granny Smith’, respectively. Vitamin C content, total phenolic compounds,
and total antioxidant capacity were determined throughout the storage period.
The results showed that all cultivars showed different responses toward
ammonium nitrogen application in terms of vitamin C content. ‘Golab Kohans’
recorded an increase in vitamin C content by increasing ammonium in nutrition
solutions. On the other hand, minor changes were recorded in ‘Granny Smith’
and Gala’. Total phenolic compounds and total antioxidant capacity were
significantly increased under all tested levels of ammonium in comparison to
control in all cultivars. Furthermore, all cultivars showed a significant decrease
in vitamin C, total phenolic compounds, and total antioxidant capacity
throughout cold storage, indicating that these bioactive compounds were
subjected to decomposition and metabolic degradation during the storage
period. Surface response analysis results showed that more vitamin C
degradation was attributed to the increase in ammonium application, while less
total phenolic compounds degradation and total antioxidant capacity decrease
were observed under similar treatments.
Keywords: Malus domestica,
Ammonium nitrate, Phenolic,
Antioxidant, postharvest
Abbreviations:
Vitamin C (VC), Total Phenolic compounds (TPC), Total Antioxidant Capacity (TAC)
1. Introduction
Apple (Malus domestica) is among the most popular, widely consumed, and cultivated fruit trees worldwide [1][2].
Apple fruits are usually consumed fresh or used in various food items such as desserts, jams, and drinks because of
their delicious taste; in addition to the remarkable attributed health benefits [3]. Many apple cultivars are known for
their ability to be stored for long periods. Due to the recent cold storage techniques, fruit markets are being supplied
by apples all year round. However, fruit quality declines during cold storage and reaches minimum levels by the end of
the storage period; especially those compounds of high nutritional values such as antioxidants and vitamins [4][5].
Taking into consideration the popular orientation toward healthier diets and wholesome foods [6], it is highly
important to investigate the factors affecting fruit quality after harvest.
DYSONA Applied Science 1 (2020) 64-72 Alhaj Alali et al.
65
In apple nutritional programs, Nitrogen levels and source type could have substantial effects on postharvest fruit
quality [7]. The unbalanced nutrition or inadequate nitrogen levels could inhibit cell division and decrease vegetative
growth, which reduces the ability of plants to produce adequate yield and fruit of high quality. Therefore, choosing the
proper rate of N fertilizer is crucial in apple production cycles [8][9].
Vitamin C (VC) is one of the highly important vitamins in the human diet because of its therapeutic and antioxidant
properties[10] as it fortifies the body defense system against free radicals and reactive oxygen species, thereby
preventing tissue damage [11][12]. Apples are considered a good source of VC as they contain considerable amounts
of this vitamin [13]. Additionally, apples have elevated phenolic compounds content [14][15], which contribute
significantly to the sensory characteristics such as color, astringent, and taste of apple cider and juice. Moreover,
phenolic compounds have previously demonstrated vigorous antioxidant properties in several systems which refers
to its cytoprotective properties [16][17]. Furthermore, apples have one of the highest levels of antioxidant activity
among fruit and vegetables [18].
N fertilization has been reported to affect phenolic content in several fruits and vegetables such as Chinese cabbage
[19]broccoli [20], and apple [21]. In the mentioned plants, an increase in phenolic content has been observed by
reducing Nitrogen application rates. Vitamin C content and antioxidative activities in Chinese cabbage were
significantly decreased with the increase in nitrogen application rates [22]. In another study, VC content was
decreased by increasing the nitrogen rate in Yellow Grape Tomato nutritional program [23].
This study aimed to investigate the effect of different levels of ammonium in the nutrition solution on vitamin C, total
phenolic compounds and total antioxidant capacity after harvest and during the cold storage period of three apple
cultivars: ‘Granny Smith’ for its known storability, Gala’, and ‘Golab Kohans’ for being widely cultivated in Iran as a
short season fruit with good marketability but low storability potentials.
2. Material and Methods
2.1. Plant material and nutrition program
The study was carried out in 2017 and 2018 seasons in the field of the Horticultural Sciences Department, University
of Tehran. The daily mean temperatures are 3˚C (average low of -1˚C and an average high of 8˚C) in winter and 25˚C
(average low of 10˚C and an average high of 34˚C) in summer. The average humidity is 65% and 35% in winter and
summer, respectively. Six years old apple trees of the cultivars ‘Golab Kohans’, ‘Gala’, and ‘Granny Smith’ grafted on
M9 rootstock and growing in 20-liter pots under open field conditions were used in this study. Five nutrition solutions
(S1, S2, S3, S4, and S5) of different ammonium to total nitrogen [NH4+/(NH4++NO3-)] were used. The ratios of
ammonium nitrogen to total nitrogen were 0, 0.08, 0.16, 0.19, and 0.27 meq/L, respectively. Trees were irrigated
three times in spring with irrigation solution, while in summer; they were irrigated once a week. Fruits were
harvested at commercial maturity on June 29th, July 21st, and September 18th for GK, G, and GS, respectively, and
transferred to cold storage at 0 ± 1 ˚C with 9095% relative humidity. Further information regarding agricultural
practices, nutrition solutions… etc. were described in [7]
2.2. Biochemical evaluation
Vitamin C (VC), total phenolic compounds (TPC) and total antioxidant capacity (TAC) were measured throughout cold
storage period at 0, 15, 30, and 45 days for GK; 0, 30, 60, and 90 days for G; and at 0, 40, 80, 120 and 160 days for
‘Granny Smith’ with three replications(three fruits per replication) for each evaluation date. Evaluation periods were
chosen due to the different storability potentials of the three cultivars i.e. ‘Golab Kohans’ having the least storage
ability and ‘Granny Smith’ having the longest storing potential.
2.2.1. Vitamin C content
VC was measured by titration with iodine and potassium iodide method. First, 16 g of potassium iodide was dissolved
in 1 liter of distilled water; then,1.27 g of iodine crystals was added and the solution was stirred on a heater. VC was
measured by adding 5 ml filtered apple juice to 20 ml distilled water and 2 ml of 1% starch solution. The formed
solution was then titrated with potassium iodide iodine solution until a dark blue color appeared. The amount of VC
was then calculated using the following formula [24]:
DYSONA Applied Science 1 (2020) 64-72 Alhaj Alali et al.
66
VC(mg/100g juice)= (0.88 × V/5) × 100
Where V is the volume of Potassium iodide iodine consumed based on ml
VC (mg/100g) = VC × [Fruit weight (g) / Fruit juice content (g)]
2.2.2. Total phenols
Measurement of phenol content in fruits was carried out using the method of [25]. The fresh fruit sample of 0.5 g was
completely crushed in 4 ml of 80% ethanol until homogenization. The homogenate was then centrifuged for 20
minutes at 9500 rounds per minute (rpm) and the clear supernatant solution was collected. In a clear tube, 8 ml
double distilled water, 1 ml Sodium carbonate 7%, and 0.5 ml Folin solution was added to 0.5 ml of the clear
supernatant fruit solution. After that, test tubes were put in a dark place for 90 minutes. Then, absorption at 625 nm
was recorded using a spectrophotometer. The total phenols content was then calculated as gallic acid equivalents
(GAE) in a Kg of fresh fruit tissue using a standard of gallic acid for absorption.
2.2.3. Total antioxidant capacity
Total antioxidant capacity was measured in the transparent extract obtained in TPC measurement. 3.4 ml of 2,2-
diphenyl-1-picrylhydrazyl (DPPH) 0.1 mM were added to 1 ml of the clear methanol extract. The mixture was kept at
room temperature and in the dark for one hour. TAC was measured based on the absorbance at a wavelength of 517
nm using a UV-Vis spectrophotometer in comparison to the standard curve. The results obtained were calculated and
expressed as the percentage of neutralized DPPH radicals (%) [26].
2.3. Statistical analysis
The study was carried out in a completely randomized block design with five treatments and 3 replications. The
experiment was repeated twice for 2017 and 2018 seasons. No significant differences were found between the studied
seasons (data not shown); therefore, the average values of two seasons were used for further analysis. Data were
analyzed using Duncan’s multiple range test (DMRT) using GenStat statistical software 17th ed. at 5% probability level.
Additionally, response surface analysis was performed between different ammonium levels and monitoring times to
investigate the interaction effect between the two variants in terms of VC, TPC, and TAC.
3. Results and Discussion
3.1. Vitamin C (mg/100g)
Figure (1A) showed that the highest VC content was at harvest for all cultivars, ‘Granny Smith’ had the highest VC
content (21.87 mg/100g) followed by ‘Gala(21.05 mg/100g) and ‘Golab Kohans’ (13.38 mg/100g). The differences in
VC of the cultivars mostly related to their genotype [27].
A significant decrease in VC was observed in ‘Golab Kohans’ cultivar by increasing nitrogen of ammonium source. The
maximum value of VC was found in S1 (control) with 13.37 mg/100g, while the minimum value was found in S5 which
recorded 9mg/100g (Table 1). On the other hand, the only noticed a significant difference in Gala’ was between S3
and S4 treatments with S4 being the highest in VC content. In GS, no significant differences were found among all
treatments. In ‘Gala’, the highest vitamin C content was observed in S4 (16.04 mg/100g), while the lowest was
recorded in S3 with a value of 14.72 mg/100g (Table 1). In ‘Granny Smith’ cultivar, the maximum value of VC was
found in apples from trees fertilized with S3 (14.19 mgl100g), while minimum value was observed in S2 which
recorded 13.75 mg/100g (Table 1). Various researches previously reported the effect of increased nitrogen
application on VC content; however, the results of those researches were contradictory as some reported a significant
increase in VC content by increasing nitrogen application, while others reported no significant differences or even
decreases in VC content [28]. VC synthesis was reported to decrease under the excessive nitrogen application as a
result of increased protein synthesis and decreased carbohydrate production which is crucial in vitamin C synthesis
[6]. The results of the current study introduce evidence of different VC synthesis response in different apple cultivars
under increased nitrogen of ammonium source application.
DYSONA Applied Science 1 (2020) 64-72 Alhaj Alali et al.
67
All cultivars showed a significant decrease in VC during the cold storage
(Table 2), which corresponds with [29] who reported more than 50% drop in
VC content of apple fruit after 6months of cold storage. Surface response
analysis demonstrated that a more pronounced decrease in VC can be seen
under high ammonium input in ‘Golab Kohans’ (Fig. 2 A) compared to the
other cultivars that exhibited less relation between ammonium input level
and VC throughout cold storage (Fig. 2 B and C). The decrease in VC content in
storage is related to its nature of being susceptible to direct or enzymatic
oxidation in comparison to other compounds during cold storage [30][31]. It
appears that high ammonium input might contribute positively to VC
degradation by participating in enzyme synthesis and/or enzymatic oxidation.
3.2. Total phenolic compounds (mg/kg)
Results showed that the highest value of TPC at harvest was for ‘Granny
Smith’ (1865 mg/kg) followed by Gala (1768 mg/kg) then ‘Golab Kohans’
(1671 mg/kg) (Fig. 1 B).
The highest values of TPC were found in S4 treatment in all cultivars with
1758, 1828, and 1942 mg/kg for GK, G, and ‘Granny Smith’, respectively;
while the minimum values were observed in S2 for ‘Golab Kohans’ (1468
mg/kg) and in S1 (control) for ‘Gala’ and ‘Granny Smith’ (1582 and 1618
mg/kg, respectively) (Table 1). It was reported that 25:75% NO3-:NH4+
treatment resulted in the highest levels of both conjugated and bound
polyamines [32], which might explain the results of the current study as
polyamines are key players in secondary metabolites synthesis including
phenolic compounds [33]. All cultivars exhibited a significant decrease in TPC
during the cold storage period (Table 2). This reduction in TPC during cold
storage appears to be genotype-dependent, as it was reported that some
genotypes undergo this degradation through cold storage [34][35][36]which
can be interpreted as the result of phenolic compounds instability during cold
storage resulting in a total metabolic degradation [35]. The surface response
model illustrated that high ammonium input in all cultivars was associated
with higher TPC and better preserving of the original phenolic compounds
content throughout storage period compared to control (Fig. 2 D, E, and F).
This effect might be attributed to ammonium water stress alleviation
potentials [37] which in turn, might result in a decreased polyphenol oxidase
(PPO) activity [38] and thus, fewer phenols degradation during the storage
period. The studied trees might have undergone a water stress status as
spring was windy and the temperature reached high values in summer at the
experiment site. This might have induced water stress even with proper
irrigation program. However, this needs further investigation.
3.3. Total antioxidant capacity (%)
The highest TAC at harvest was recorded in ‘Granny Smith’ (71.31%)
followed by ‘Golab Kohans’ (68.04%) then ‘Gala’ (67.61%) (Fig. 1 C).
In regards to ammonium application, S4 gave the highest TAC for both ‘Gala
and ‘Granny Smith’ cultivars, while S3 and S5 gave the highest TAC in ‘Golab
Kohans’ cultivar. On the other hand, the lowest TAC values were observed
under S1 treatment for all cultivars (Table 1). Similar to TPC, TAC response
surface contour plotting illustrated that nutrition solutions with higher
ammonium levels resulted in a better maintaining of antioxidant capacity
Figure 1. Effect of Cultivar on Vitamin C
(mg/100g) (A), total phenols (mg/kg) (B),
and total antioxidant (%) (C) in the fruits
of ‘Golab Kohans’, Gala’, and ‘Granny
Smith’ apple cultivars at harvest.
Total Phenolic compounds contents were
expressed as gallic acid equivalents (GAE)
in a Kg of fresh fruit tissue.
Total antioxidant capacity was expressed
as the percentage of neutralized DPPH
radicals.
* Values were represented as an average
for all treatments at harvest (regardless of
ammonium input).
DYSONA Applied Science 1 (2020) 64-72 Alhaj Alali et al.
68
throughout cold storage period compared to non-ammonium nutrition solution (control) and in all cultivars (Fig. 2 G,
H, and I). However, ‘Golab Kohans’ showed a more sharp decrease under control treatment (Fig. 2 G). The significant
increase in TAC under all ammonium treatments and for all cultivars in comparison to non-ammonium control
treatment (S1) might be attributed to the accumulation of polyamines due to the high ammonium concentrations
[36][39]resulting in the activation of various plant defense mechanisms [40] including antioxidants [33].
All cultivars showed a significant decrease in TAC with each measurement throughout the cold storage period (Table
2) which is due to the decomposition of antioxidants throughout the storage period [41].
Figure 2. Surface analysis contour plotting for the relationship between ammonium content in nutrition solution and
cold storage time for vitamin C content (VC) (mg/100g) (A, B, and C), total phenolic compounds (TPC) (mg/Kg) (D, E,
and F), and total antioxidant capacity (TAC) (%) (G, H, and I) in the three studied apple cultivars: ‘Golab Kohans’(A,
D, and G),‘Gala(B, E, and H), and ‘Granny Smith’(C, F, and I).
Total phenolic compounds content were expressed as gallic acid equivalents (GAE) in a Kg of fresh fruit tissue
Total antioxidant capacity was expressed as the percentage of neutralized DPPH radicals
4. Conclusion
The results of this study showed that the cultivars exhibited different responses toward ammonium nitrogen
application in terms of VC content. ‘Golab Kohans’ recorded an increased VC content by increasing ammonium in the
nutrition solution. On the other hand, minor or no changes were observed in ‘Gala’ and 'Grany Smith'. TPC and TACin
all cultivars were significantly increased under any ammonium input in comparison to control treatment.
Furthermore, all cultivars underwent a significant decrease in VC, TPC, and TAC throughout cold storage. Surface
response analysis results illustrated that with the increase in ammonium inputs, more vitamin C degradation was
observed. On the other hand, less TPC degradation and TAC decreasing were recorded under similar conditions.
DYSONA Applied Science 1 (2020) 64-72 Alhaj Alali et al.
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Cultivar
N treatment
Vitamin C
(mg/100g)
total phenolic
compounds (mg/kg)A
total antioxidant
capacity%B
Golab
Kohans
S1
13.37a
1482d
51.39d
S2
12.70b
1468d
61.72c
S3
10.74c
1710b
65.44a
S4
9.85d
1758a
62.90b
S5
9.00e
1650c
65.64a
Gala
S1
15.35ab
1582d
51.46c
S2
15.21ab
1622c
52.53c
S3
14.72b
1708b
61.24b
S4
16.03a
1828a
65.53a
S5
15.05ab
1695b
62.38b
Granny smith
S1
14.09a
1618d
56.81e
S2
13.75a
1648c
58.11d
S3
14.19a
1774b
64.98b
S4
14.04a
1942a
67.56a
S5
14.14a
1786b
61.29c
Different letters in each column for each cultivar indicate significant differences using Duncan multiple range test (P≤0.05)
A, Total phenolic compounds content were expressed as gallic acid equivalents (GAE) in a Kg of fresh fruit tissue.
B, Total antioxidant capacity was expressed as the percentage of neutralized DPPH radicals
Cultivar
Storage time (days)
Vitamin
C(mg/100g)
total phenolic
compounds (mg/kg)A
total antioxidant
capacity%B
Golab
Kohans
0
13.38a
1671a
68.04a
15
12.20b
1631b
63.99b
30
10.51c
1594c
58.95c
45
8.45d
1557d
54.68d
Gala
0
21.05a
1768a
67.61a
30
16.91b
1718b
62.18b
60
14.40c
1658c
55.62c
90
8.72d
1603d
49.10d
Granny smith
0
21.87a
1865a
71.31a
40
17.26b
1815b
67.90b
80
14.07c
1755c
62.39c
120
8.59d
1690d
56.74d
160
8.42d
1645e
50.40e
Different letters in each column for each cultivar indicate significant differences using Duncan multiple range test (P≤0.05)
A, Total phenolic compounds content were expressed as gallic acid equivalents (GAE) in a Kg of fresh fruit tissue
B, Total antioxidant capacity was expressed as the percentage of neutralized DPPH radicals
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