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Journal of Food Quality ISSN 1745-4557
PHYSICOCHEMICAL PARAMETERS AND ANTIOXIDANT COMPOUNDS IN EDIBLE SQUASH (CUCURBITA PEPO) FLOWER STORED UNDER CONTROLLED ATMOSPHERES E.N. AQUINO-BOLAÑOS1,3, T.A. URRUTIA-HERNÁNDEZ1, M. LÓPEZ DEL CASTILLO-LOZANO1, J.L. CHAVÉZ-SERVIA2 and I. VERDALET-GUZMÁN1 1
Posgrado en Ciencias Alimentarias, Instituto de Ciencias Básicas, Universidad Veracruzana. Av. Dr. Rafael Sánchez Altamirano S/N, Industrial Animas, Xalapa, Veracruz 91192, Mexico 2 CIIDIR-Oaxaca, Instituto Politécnico Nacional, Santa Cruz Xoxocotlán, Oaxaca, Mexico
3
Corresponding author. TEL: +52-228-8418931; FAX: +52-228-8418932; EMAIL:
[email protected] Received for Publication January 7, 2013 Accepted for Publication August 2, 2013 10.1111/jfq.12053
ABSTRACT Edible squash (Cucurbita pepo) flower is highly in demand in Mexico and internationally, but its high perishability limits marketing. An evaluation of the effect of storage under controlled atmosphere (CA) on physicochemical parameters and antioxidant compounds contents in squash flower was carried out. Male flowers were stored at 5C under a continuous flow of gas with one of four compositions: 5% O2 + N2 (CA1); 5% O2 + 10% CO2 + N2 (CA2); 10% CO2 + air (CA3); and air as a control. Compared with the control, the CA treatments had greater retention of total sugars, total soluble solids, pH, titratable acidity and lower physiological weight loss. At 16 days, CA2 retained the highest amount of ascorbic acid (49.5%), polyphenols (65.2%) and carotenoids (72.8%). Application of CA2 or CA3 could prolong postharvest life in squash flowers up to 16 days.
PRACTICAL APPLICATIONS Squash plants are monoecious, bearing male and female flowers on the same plant. Female flowers produce the fruit, while male flowers are edible and used widely in a number of dishes, but their short shelf life limits marketability. The results demonstrate that storage of squash flowers in atmospheres with high (10%) CO2 concentration prolongs shelf life up to 16 days.
INTRODUCTION Edible flowers include tens of inflorescences of different shapes, colors and sizes used around the world to improve the appearance, color and nutritional value of foods (Kelley et al. 2001). In general, edible flowers are also known to be a good source of antioxidant compounds (Mlcek and Rop 2011). The bright yellow color, soft texture and delicate, slightly sweet flavor of squash (Cucurbita pepo) flowers have made them a favorite ingredient in the U.S.A., Europe and Asia (Tarhan et al. 2007). They are a rich source of minerals, vitamins B1 and B2, folic acid and essential amino acids (Talavera 1999; Sotelo et al. 2007), as well as antioxidant compounds such as ascorbic acid (Aa), polyphenols and carotenoids (UrrutiaHernández 2011). 302
Most edible flowers used in Mexico are collected and consumed locally during the blooming period, and only squash flower is highly in demand all year round. It is used in salads, dressings, soups and main dishes, but it is most frequently used in quesadillas (corn or wheat tortillas filled with melted cheese and squash flowers) (Sotelo et al. 2007), in crepes in French cuisine and in pasta in Italian cuisine. Its short shelf life is the main factor limiting marketing of squash flower. Because of its high respiratory rate, a squash flower remains fresh for one day at room temperature (Villalta et al. 2004). The changes associated with postharvest deterioration in edible flowers have been scarcely studied. In a study of Viola tricolor L., Viola wittrockiana L., Tropaeolum majus L., Borago officinalis L. and Phaseolus coccineus flowers stored at low density in polyethylene bags at −2.5 and 20C for 2 weeks, Kelley et al. (2003) reported Journal of Food Quality 36 (2013) 302–308 © 2013 Wiley Periodicals, Inc.
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signs of necrosis, tissue collapse and fungi. In another study, storage of squash flowers in polypropylene containers at 2.5 and 5C conserved appearance for 7 days (Villalta et al. 2004), although this is insufficient time for marketing. Further research using different technologies is still needed to extend squash flower shelf life. Controlled atmospheres (CAs) are used in addition to refrigeration to extend postharvest shelf life in fruits and vegetables. This technology involves modification of air composition, keeping O2 concentrations low and CO2 concentrations high, thus reducing respiration rate, decreasing enzymatic activity and diminishing the changes associated with senescence (Kader 1985; Yahia 1998). The present study objective was to evaluate the effect of storage under CAs on squash flower physicochemical parameters and antioxidant compound levels.
MATERIALS AND METHODS Biological Material Squash (Cucurbita pepo var. Grey zucchini) seeds were planted and cultivated under greenhouse conditions (Training Unit for Rural Development # 2, Coatepec, Veracruz, Mexico). At 50 days, completely open and homogenous color, mature male flowers were harvested.
Storage Conditions The selected flowers were stored in a cold room at 5 ± 1C. Twelve flowers were placed in a punnet and four punnets placed in each 20-L glass container. A continuous flow of humidified gas (relative humidity = 95–98%) was maintained in these containers and four atmospheres were used: 5% O2 + N2 (CA1); 5% O2 + 10% CO2 + N2 (CA2); 10 % CO2 + air (CA3); and 100% air as a control. The CAs were produced by mixing the appropriate volumes of oxygen, carbon dioxide, air and nitrogen (N2 was used to complete volume to 100%). Oxygen and CO2 concentrations within the containers were recorded daily with a gas analyzer (PBI Dansensor, Checkpoint, Denmark) to ensure that gas proportions were correct. Every four days, flower corolla samples were taken and analyses run of total sugars (TS), total soluble solids (TSS), titratable acid (TA), pH, Aa, phenolic compounds, total carotenoids and antioxidant activity. Physiological weight loss and visual quality were measured using whole flowers (corolla + stem) at the same intervals. Three replicates of six flowers each were analyzed per treatment/time.
METHODS TS content was determined following the phenolsulfuric acid method (Dubois 1956). Briefly, 1 g tissue was Journal of Food Quality 36 (2013) 302–308 © 2013 Wiley Periodicals, Inc.
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homogenized (Wisd Laboratory Instruments, Wertheim, Germany) with 30 mL of 80% ethanol (v/v) and stored at −20C for 24 h. This solution was then filtered, 300 μL was mixed with 100 μL of 80% phenol (v/v) and 5 mL of concentrated H2SO4. The mixture was incubated for 20 min at 30C and absorbance read at 490 nm with a spectrophotometer (Jenway 6305, Staffordshire, U.K.). TS content was quantified using a standard glucose curve (0.01– 0.12 mg/mL). To determine TSS, 2 g tissue was homogenized with 8 mL of distilled water, filtered and the solution read directly as °Brix with a digital refractometer (ATAGO PR-32, Tokyo, Japan). Changes in pH and TA were analyzed following standard methods (AOAC 1999). Briefly, 4 g sample was homogenized in 36 mL of distilled water, filtered and pH measured with a potentiometer (OAKTON 510, Malaysia). TA was measured by titrating 10 mL of this solution with 0.01 N NaOH and using phenolphthalein as an indicator. Aa content was determined using 2,6-dichloroindophenol following standard methods (AOAC 1999). Phenolic compound content was analyzed with Folin–Ciocalteu reagent according to the method of Singleton and Rossi (1965). Quantification was carried out using a standard gallic acid curve (0.02–0.12 mg/mL). Carotenoid content was determined by grinding 1 g tissue with 5 g anhydrous Na2SO4 in a mortar. This mixture was extracted twice with 20 mL acetone : hexane (1:1, v/v) solution, and the sum of the extracts run through a separation funnel to eliminate the acetone with 200 mL of distilled water. The acetone-free phase was mixed with 5 g anhydrous Na2SO4 to eliminate any residual water, the remaining solution filtered and completed to 100 mL with hexane (Rodríguez-Amaya and Kimura 2004). Carotenoid content was determined by reading absorbance at 450 nm and comparing results to a β-carotene calibration curve (2–18 μg/mL). Antioxidant activity was measured following the DPPH (2,2-diphenil-1-picrylhydrazyl) method of Brand-Williams et al. (1995). Briefly, 3 g tissue was homogenized with 30 mL of 80% ethanol (v/v) and the extract filtered. From this filtered fraction, 100 μL was taken and mixed with 2,900 μL DPPH reagent (3.9 mg/100 mL in methanol), and the mixture left to incubate at room temperature for 30 min. Absorbance was then read at 517 nm and contents quantified by comparison with a standard Aa curve (0.3– 1.5 μmol Aa equivalent/mL). Physiological weight loss was recorded by measuring the weight (balance ± 0.01 g) of four flowers per treatment at the beginning of storage and every day of the storage period. Results were expressed as a percentage of the initial weight. Evaluation of overall visual quality was performed by expert grading. In this method, a small group of highly trained or experienced individuals (generally two to five) 303
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use selected scales (typically 5–10 points) labeled with descriptors for at least half the points (Shewfelt 2003). For this study, the panel consisted of five judges from the Basic Science Institute of the Universidad Veracruzana who were familiar with squash flower characteristics. Overall visual quality was evaluated on a 9-to-1 scale: 9 = excellent, no defects; 7 = good, minor defects; 5 = fair, moderate defects; 3 = poor, major defects; 1 = unusable. A score of 6 was considered the limit of marketability.
Statistical Analyses Data were processed with an analysis of variance and a Tukey comparison of means (P < 0.05). A Pearson correlation coefficient was run for the study variables. All statistical analyses were carried out using the XLSTAT ver. Pro 7.5 program (Addinsoft Inc., Paris, France).
RESULTS AND DISCUSSION Physicochemical Properties Initial TS content was 713 mg/100 g, which decreased during storage in all treatments. This is to be expected as flower petals accumulate sugars during plant development, and after being cut, these sugars (mostly soluble) are the main substrate used for respiration during postharvest storage (Maness and Perkins-Veazie 2003). Sugar consumption was lower in the CA treatments compared with the control (Fig. 1A); e.g., at day 8, CA1 retained 29% of initial TS content, CA2 retained 75% and CA3 retained 37%, while the control retained only 17%. At the end of the storage period, CA2 retained 47.5% of TS, followed by CA3 with 32.6%. The higher sugar stability in the CA treatments may be linked to a reduction in metabolism-associated enzyme activity (McKenzie et al. 2004). In a 10% CO2 atmosphere, activity decreases for phosphofructokinase, one of the two enzymes that regulate glycolysis (Kerbel et al. 1990). A similar phenomenon may have occurred in the CA2 and CA3 treatments, which would explain the reduced sugar consumption rate. Low O2 concentrations are also known to diminish the activity of dehydrogenase pyruvate, an enzyme complex that catalyzes pyruvate conversion to acetyl-CoA, the main entrance for sugars into the Krebs cycle. This could explain the decrease in changes associated with sugar degradation in CA1 (5% O2 + N2). The highest sugar retention levels were observed in CA2, at a high CO2 concentration and low O2 concentration. Recently, harvested flowers exhibited 4.57°Brix, although this quickly dropped to 1.61°Brix at day 8 in the control treatment (Table 1). By contrast, TSS in the CA2 treatment only differed (P < 0.05) from the initial content at day 16 304
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(3.61°Brix). TSS content correlated with TS (R = 0.91) and TA (R = 0.91). Stability of TSS under high CO2 and low O2 atmospheres has been reported for tissues such as cabbage (Rinaldi et al. 2010). TA decreased during storage in all treatments (initial = 0.22 g citric acid/100 g), the lowest reduction being in CA2 (Table 1). These levels may be explained by the fact that after harvest products with relatively low reserve substrate, such as flowers and leaves, use organic acids as a substrate for respiration (Teixeira da Silva 2003). Initial pH in the squash flowers was slightly acidic (pH = 5.79), but increased in value during storage. At days 4 and 8, CA1 exhibited the highest acid retention (Table 1). This increase in pH correlated with decreases in TA (R = 0.85).
Antioxidant Compounds Aa is the principal antioxidant compound found in plants and is an essential nutrient for humans. In all the treatments, Aa content decreased during storage (Table 2). This can be explained by the fact that Aa is found in the extracellular aqueous phase, in the cytosol and mitochondria (Loewus 1988). However, when cell integrity is lost, the organs decompartmentalize, causing release and exposure of Aa to atmospheric oxygen. In this medium, Aa degradation is produced by its strong reducing or antioxidant potential, which, by displacing [H+], prepares the molecule to combat free radicals (•O2, •OH and •H2O2) (Noctor and Foyer 1998). It is therefore to expected that Aa loss was lowest in the CA treatments; at day 8, Aa was 74% of initial content in CA1, 71% in CA2 and 66% in CA3, but only 55% in the control. At day 16, CA2 retained the higher percentage (49.5%) of Aa than CA3 (44.8%). Initial phenolic compound content in squash flower (334.6 mg/100 g) was much higher than reported for vegetables such as cabbage (25 mg/100 g), parsley (20–40 mg/ 100 g) and celery (94 mg/100 g) (Bravo 1998). However, it decreased during storage; at day 8, CA1 and CA3 had higher concentrations than AC2 and control (Table 2). Carotenoids are responsible for the yellow/orange color of squash flowers, with zeaxanthin, flavoxanthin and cryptoxanthin being the main carotenoids in C. pepo (Azimova and Glushenkova 2012). The recently harvested flowers had a 76.83 mg/100 g carotenoid content, which is higher than the 1.23–18.79 mg/100 g reported for pumpkin (Cucurbita maxima) flowers (Seroczynska et al. 2006). By day 4, carotenoid content had begun to decrease, and by day 8, it was at 72% in CA1, 88% in CA2, 76% in CA3 and 57% in the control (Fig. 1B). At day 16, CA2 retained 72.8% of initial carotenoid contents. In products containing chlorophyll or carotenoids, color degradation occurs through a co-oxidation mechanism in Journal of Food Quality 36 (2013) 302–308 © 2013 Wiley Periodicals, Inc.
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A
1000
B
80
70
AC3 (10% CO2 + Air) Air
60
600
50
400 40
200 10
0
0
12
C
D
9
10
7
8 %
mg β-carotene/ 100 g FW
AC2 (5% O2 + 10% CO2 + N2)
800
6
5 4
3
2
9 = excellent; 1 = unusable
mg glucose/ 100 g FW
AC1 (5% O2 + N2)
0
1 0
4
8
12
16
Days after storage
0
4
8
12
16
Days after storage
FIG. 1. TOTAL SUGARS (A), CAROTENOIDS (B), PHYSIOLOGICAL WEIGHT LOSS (C) AND VISUAL QUALITY (D) IN SQUASH FLOWER DURING POSTHARVEST STORAGE UNDER CONTROLLED ATMOSPHERES
which pigments are destroyed by the attack of free radicals produced by the action of the enzyme lipoxygenase on fatty acids (Jarén-Galán and Mínguez-Mosquera 1997). Lipoxygenase activity decreases at low O2 concentrations, possibly explaining the greater carotenoid stability in CA1. In addition, carotenoid loss was less in the treatments with higher Aa contents (CA1, CA2 and CA3). This was possibly in response to the high reducing capacity of the Aa protecting the fatty acids from lipoxygenase (Horemans et al. 2000), therefore reducing free radical release and consequent carotenoid degradation. This coincides with the high correlation (R = 0.94) observed between Aa levels and carotenoid contents. Journal of Food Quality 36 (2013) 302–308 © 2013 Wiley Periodicals, Inc.
Antioxidant compounds are vital to flowers because they inhibit the senescence processes caused by the action of oxygen reactive species in biomembranes (Panavas and Rubinstein 1998). Initial antioxidant activity in the squash flowers was 62 μmol Aa equivalent/100 g, but by day 8, it had dropped to 48.99 μmol in CA1, 43.63 μmol in CA2, 46.87 μmol in CA3 and 37.86 μmol Aa equivalent/100 g in the control (Table 2). The drastic drop in antioxidant activity in the control treatment may be due to free radical production during respiration (Yao et al. 2004), which can be controlled with enzymes and antioxidant compounds, such as Aa, carotenoids and polyphenols (Que et al. 2007). When free radical concentration exceeds antioxidant action 305
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Total soluble solids (°Brix) Day/treatment 0 4 8 12 16
Control (air)
CA1
CA2
CA3
4.57 ± 0.30aA 2.87 ± 0.21bB 1.61 ± 0.15cC
4.57 ± 0.30aA 3.27 ± 0.19bB 3.10 ± 0.27bcB 2.59 ± 0.41cB
4.57 ± 0.45aA 4.11 ± 0.42aA 4.06 ± 0.30aA 4.13 ± 0.36aA 3.61 ± 0.15bA
4.57 ± 0.30aA 4.47 ± 0.23aA 4.09 ± 0.35aA 3.38 ± 0.43bA 2.53 ± 0.18cB
TABLE 1. TOTAL SOLUBLE SOLIDS, TITRATABLE ACIDITY AND pH IN SQUASH (CUCURBITA PEPO) FLOWER DURING POSTHARVEST STORAGE UNDER CONTROLLED ATMOSPHERES
Titratable acidity (g citric acid/100 g FW) Day/treatment 0 4 8 12 16
Control (air)
CA1
0.220 ± 0.029 0.118 ± 0.033bB 0.055 ± 0.030cC
aA
CA2
0.220 ± 0.029 0.120 ± 0.040bB 0.094 ± 0.008cB 0.087 ± 0.007cB
aA
CA3
0.220 ± 0.029 0.171 ± 0.019bA 0.120 ± 0.009cA 0.113 ± 0.008cA 0.098 ± 0.016cA aA
0.220 ± 0.029aA 0.153 ± 0.090bAB 0.106 ± 0.008cAB 0.076 ± 0.004dB 0.043 ± 0.009eB
pH Day/treatment 0 4 8 12 16
Control (air)
CA1
CA2
CA3
5.79 ± 0.14cA 6.46 ± 0.07bA 7.17 ± 0.05aA
5.79 ± 0.14cA 6.01 ± 0.08bC 6.15 ± 0.04bD 6.80 ± 0.05aA
5.79 ± 0.14dA 6.38 ± 0.08cB 6.51 ± 0.06cC 6.71 ± 0.05bA 7.49 ± 0.06aA
5.79 ± 0.14cA 6.66 ± 0.04bA 6.86 ± 0.09bB 6.89 ± 0.12bA 7.45 ± 0.15aA
a,b
Means in the same column with a different lowercase letter are significantly different (P < 0.05). A,B Means in the same row with a different uppercase letter are significantly different (P < 0.05). CA1: 5% O2 + N2; CA2: 5% O2 + 10% CO2 + N2; CA3: 10 % CO2 + air. FW, fresh weight.
capacity, oxidative stress begins, leading to a series of irreversible changes such as loss of cellular integrity, senescence and flower death (Bartoli et al. 1995). There was a high correlation in the present study between antioxidant activity and polyphenols (R = 0.96) and Aa (R = 0.97) contents, but a lower correlation with carotenoid content (R = 0.87).
Physiological Weight Loss and Visual Quality Physiological weight loss has been linked to decreases in substrates such as the sugars and organic acids used during postharvest respiration (Wills et al. 1998). By day 8 of storage in the present study, the squash flowers had lost 3.26% of their weight in CA1, 2.35% in CA2, 1.61% in CA3 and 7.67% in the control (Fig. 1C). By day 16, weight loss was 4.57% and 5.18% in CA2 and CA3, respectively. Decreases in weight loss over time during storage compared with a control (storage in air) have also been reported for broccoli stored in 5% O2 and 10% CO2 (Eason et al. 2007). Recently harvested squash flowers received a score of 9 for overall visual quality, meaning their corollas were intact and coloring was uniform. For flowers in the CA treatments, this score remained unchanged until day 4, while 306
flowers in the control were scored at 7.3 (Fig. 1D). By day 8, the flowers in the control had reached the minimum score (6) for marketing. In contrast, those in the CA2 (7.6) and CA3 (7.7) treatments still exhibited only minor objectionable defects by day 16. The results show that the CAs, particularly those with high CO2 concentrations (CA2 and CA3), diminished the rate at which the biochemical reactions associated with cellular degradation occurred, resulting in a higher postharvest shelf life compared with the control treatment.
CONCLUSIONS Squash flowers stored under CAs after harvest manifested minor changes in the physicochemical properties and antioxidant compound retention. As a result, overall visual quality remained acceptable up to 12 days in 5% O2 + N2 (CA1) and up to 16 days in 5% O2 + 10% CO2 + N2 (CA2) and 10 % CO2 + air (CA3). Flowers stored under a normal atmosphere remained marketable up to 8 days. Use of CAs with high CO2 and low O2 concentrations clearly extended squash flower shelf life, opening the possibility of larger potential markets for this raw material. Journal of Food Quality 36 (2013) 302–308 © 2013 Wiley Periodicals, Inc.
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TABLE 2. ASCORBIC ACID, POLYPHENOLS AND ANTIOXIDANT ACTIVITY IN SQUASH (CUCURBITA PEPO) FLOWER DURING POSTHARVEST STORAGE UNDER CONTROLLED ATMOSPHERES
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Ascorbic acid (mg/100 g FW) Day/Treatment 0 4 8 12 16
Control (air)
CA1
CA2
CA3
16.51 ± 0.34aA 11.23 ± 0.39bB 9.09 ± 0.12cC
16.51 ± 0.34aA 14.31 ± 0.32bA 12.21 ± 0.71cA 8.12 ± 0.32dB
16.51 ± 0.34aA 14.44 ± 1.11bA 11.75 ± 0.69cA 11.53 ± 0.14cA 8.17 ± 0.28dA
16.51 ± 0.34aA 13.36 ± 0.29bA 10.88 ± 0.16cB 8.31 ± 0.30dB 7.39 ± 0.15eB
Total phenolics (mg gallic acid/100 g FW) Day/Treatment
Control (air)
CA1
334.6 ± 18 269.6 ± 8bB 238.4 ± 21bB
334.6 ± 18 322.6 ± 14aA 293.2 ± 12bA 232.7 ± 14cA
aA
0 4 8 12 16
CA2 aA
CA3
334.6 ± 18 321.7 ± 10aA 261.2 ± 10bB 248.5 ± 5bA 218.1 ± 8cA aA
334.6 ± 18aA 308.6 ± 12abA 301.3 ± 9bA 220.3 ± 26cA 209.3 ± 8cA
Antioxidant activity (μmol ascorbic acid equivalent/100 g FW) Day/Treatment 0 4 8 12 16
Control (air)
CA1
CA2
CA3
62.00 ± 3.61aA 39.42 ± 4.04bB 37.86 ± 1.24bC
62.00 ± 3.61aA 52.88 ± 1.71bA 48.99 ± 2.34bA
62.00 ± 3.61aA 56.67 ± 4.62aA 43.63 ± 1.00bB 39.99 ± 1.27cA 38.95 ± 0.76cA
62.00 ± 3.61aA 54.55 ± 1.23bA 46.87 ± 3.98cAB 41.25 ± 1.93cA
a,b
Means in the same column with a different lowercase letter are significantly different (P < 0,05). A,B Means in the same row with a different uppercase letter are significantly different (P < 0.05). AC1:5% O2 + N2; AC2: 5% O2 + 10% CO2 + N2; AC3: 10 % CO2 + air. FW, fresh weight.
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Journal of Food Quality 36 (2013) 302–308 © 2013 Wiley Periodicals, Inc.