Preharvest Application of Oxalic Acid Increased Fruit Size, Bioactive

Article pubs.acs.org/JAFC

Preharvest Application of Oxalic Acid Increased Fruit Size, Bioactive Compounds, and Antioxidant Capacity in Sweet Cherry Cultivars (Prunus avium L.) Alejandra Martínez-Esplá,† Pedro Javier Zapata,† Daniel Valero,† Cristina García-Viguera,‡ Salvador Castillo,† and María Serrano*,§ †

Department of Food Technology, EPSO, University Miguel Hernández, Ctra. Beniel km. 3.2, 03312 Orihuela, Alicante, Spain Department of Food Science and Technology, CEBAS-CSIC, Campus Espinardo, 30100 Murcia Spain § Department of Applied Biology, EPSO, University Miguel Hernández, Ctra. Beniel km. 3.2, 03312 Orihuela, Alicante, Spain ‡

ABSTRACT: Trees of ‘Sweet Heart’ and ‘Sweet Late’ sweet cherry cultivars (Prunus avium L.) were treated with oxalic acid (OA) at 0.5, 1.0, and 2.0 mM at 98, 112, and 126 days after full blossom. Results showed that all treatments increased fruit size at harvest, manifested by higher fruit volume and weight in cherries from treated trees than from controls, the higher effect being found with 2.0 mM OA (18 and 30% higher weight for ‘Sweet Heart’ and ‘Sweet Late’, respectively). Other quality parameters, such as color and firmness, were also increased by OA treatments, although no significant differences were found in total soluble solids or total acidity, showing that OA treatments did not affect the on-tree ripening process of sweet cherry. However, the increases in total anthocyanins, total phenolics, and antioxidant activity associated with the ripening process were higher in treated than in control cherries, leading to fruit with high bioactive compounds and antioxidant potential at commercial harvest (≅45% more anthocyanins and ≅20% more total phenolics). In addition, individual anthocyanins, flavonols, and chlorogenic acid derivatives were also increased by OA treatment. Thus, OA preharvest treatments could be an efficient and natural way to increase the quality and functional properties of sweet cherries. KEYWORDS: oxalic acid, preharvest treatment, quality, phenolics, flavonols, anthocyanins, total antioxidant activity

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INTRODUCTION Sweet cherry is one of the fruits most appreciated by consumers due to its precocity and excellent quality, the main quality attributes being fruit weight, color, firmness, sweetness, sourness, flavor, and aroma.1−3 However, sweet cherry fruits are appreciated not only for their sensory and nutritional properties but also for their content in bioactive compounds with additional health benefits.4,5 In this sense, it has been reported that sweet cherry fruit holds potential for the prevention of cancer, cardiovascular disease, diabetes, and other inflammatory diseases through reduction of oxidant stress, inflammation or tumor suppression, glucose control, and inhibition of uric acid production.5,6 Among these bioactive compounds, in sweet cherry, special interest has been focused on anthocyanins and polyphenols, due to their antioxidant properties, which showed important differences among cultivars, ripening stage, and storage conditions.2,3,7−10 Oxalic acid (OA), as a final metabolite product in plants, has many physiological functions, the main one being related to the induction of systemic resistance against diseases caused by fungi, bacteria, and viruses, by increasing defense-related enzyme activities and secondary metabolites, such as phenolics.11 In addition, postharvest treatments with OA were effective in delaying the ripening process in some climacteric fruits, such as mango,12 plum,13 peach,14 and jujube fruit,15 through an inhibition of ethylene biosynthesis. Another beneficial effect of postharvest OA treatment is decreased chilling injury (CI) symptoms in sensitive fruits, such as pomegranate,16 litchi,17 and mango.18 In addition, in sweet © 2014 American Chemical Society

cherry postharvest OA treatment also delayed the postharvest ripening process, manifested by lower acidity and firmness losses and color changes, leading to maintenance of fruit quality attributes for longer periods in treated fruits than in controls, with the additional benefit of maintaining higher levels of antioxidant compounds.19 However, no literature is available about the effect of preharvest OA treatment on fruit development, ripening, or quality attributes at harvest time, which has been the main objective of this paper, with special interest in bioactive compounds, such as anthocyanins and phenolics, and antioxidant activity. In addition, the effect of preharvest OA treatment on individual anthocyanins, flavonols, and chlorogenic acid derivatives at harvest was also analyzed.

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MATERIALS AND METHODS

Plant Material and Experimental Design. For this study, two sweet cherry (Prunus avium L.) cultivars, ‘Sweet Heart’ and ‘Sweet Late’, were used, which are late-season cultivars with high quality attributes and appreciated by consumers. The experiment was carried out during the developmental cycle of the 2013 spring−summer period, in a commercial plot of Fincas Toli S.L. located at Jumilla (Murcia, Spain). For both cultivars, date for full blossom was February 20. Three trees were selected for each cultivar and treatment: control (distilled water) and oxalic acid (OA) at three concentrations (0.5, 1.0, and 2.0 mM). OA was purchased from Sigma (Sigma-Aldrich, Madrid, Received: Revised: Accepted: Published: 3432

January 15, 2014 March 25, 2014 March 31, 2014 March 31, 2014 dx.doi.org/10.1021/jf500224g | J. Agric. Food Chem. 2014, 62, 3432−3437

Journal of Agricultural and Food Chemistry

Article

Figure 1. Fruit volume (mm3) during on-tree fruit development of ‘Sweet Heart’ and ‘Sweet Late’ sweet cherry cultivars treated with oxalic acid (OA, 0.5, 1.0, or 2.0 mM) at 98, 112, and 126 days after full blossom (T1, T2, and T3). Data are the mean ± SE. 10000g for 15 min at 4 °C. The upper fraction was used for total antioxidant activity due to lipophilic compounds (L-TAA) and the lower fraction for total antioxidant activity due to hydrophilic compounds (H-TAA). In both cases, TAA was determined using the enzymatic system composed of the chromophore 2,2′-azinobis(3ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), the horseradish peroxidase enzyme (HRP), and its oxidant substrate (hydrogen peroxide, H2O2), in which ABTS•+ radicals are generated and monitored at 730 nm. The reaction mixture contained 2 mM ABTS, 15 μM H2O2, and 25 μM HRP in 50 mM sodium phosphate buffer (pH 7.8) in a total volume of 1 mL. The decrease in absorbance after adding the extract was proportional to the TAA of the sample. A calibration curve was performed with Trolox ((R)-(+)-6-hydroxy2,5,7,8-tetramethylchroman-2-carboxylic acid) (0−20 nmol) from Sigma (Madrid, Spain), and results are expressed as milligrams of Trolox equivalent per 100 g of fresh weight. Bioactive Compound Determination. Total phenolics were extracted according to the Tomás-Barberán et al. protocol20 using water/methanol (2:8) containing 2 mM NaF (to inactivate polyphenol oxidase activity and prevent phenolic degradation) and quantified in duplicate using the Folin−Ciocalteu reagent, and results (mean ± SE) were expressed as milligrams of gallic acid equivalent per 100 g of fresh weight. Total anthocyanins were determined according to the method of Garcı ́a-Viguera et al.21 adapted as previously reported10 and calculated as cyanidin 3-glucoside equivalent (molar absorption coefficient of 23900 L cm−1 mol−1 and molecular weight of 449.2 g mol−1), and results were expressed as milligrams per 100 g of fresh weight and were the mean ± SE. For individual phenolic compounds, the protocol described by Gironés-Vilaplana et al. was followed.22 Briefly, lyophilized samples (100 mg) were mixed with 1 mL of methanol/formic acid/water (25:1:24, v/v/v), vortexed, sonicated in an ultrasonic bath for 60 min, and centrifuged at 10500g for 5 min. The supernatant was filtered through a 0.45 μm PVDF filter (Millex HV13, Millipore, Bedford, MA, USA) and used for HPLC analysis. The HPLC system was equipped with a Luna C18 column (25 cm × 0.46 cm i.d., 5 μm particle size; Phenomenex, Macclesfield, UK) with a C18 security guard (4.0 × 3.0 mm) cartridge system (Phenomenex). Water/formic acid (99:5, v/v) and acetonitrile were used as mobile phases A and B, respectively, with a flow rate of 1 mL/min. The linear gradient started with 8% of solvent B, reaching 15% of solvent B at 25 min, 22% at 55, and 40% at 60 min, which was maintained up to 70 min. The injection volume was 20 μL. Chromatograms were recorded at 280, 320, 360, and 520 nm. Different phenolics were characterized by chromatographic comparison with analytical standards as well as quantified by the absorbance of their corresponding peaks.

Spain). Freshly prepared solutions (containing 0.5% Tween 20) were foliar sprayed with a mechanical mist sprayer and repeated at three dates of the growth cycle: T1 (at pit hardening, 98 days after full blossom, DAFB), T2 (initial color changes, 112 DAFB), and T3 (onset of ripening, 126 DAFB). These dates corresponded to key events in the fruit developmental process, according to previous experiments.3 Before T1 treatment, 20 fruits were labeled around the equatorial perimeter of each tree, in which fruit growth was followed by measuring polar, suture, and cheek diameters, and then fruit volume was calculated as previously reported.3 On a weekly basis, from 1 week before the T1 treatment to commercial harvesting, 20 fruits (similar to those labeled) for each tree (or replicate) were picked for further analytical determinations: fruit firmness, color, total soluble solids (TSS), and total acidity (TA). In addition, the content of bioactive compounds (total phenolics and total anthocyanins) and total antioxidant activity were determined in fruits from control and 2.0 mM OA treated trees. In these fruits, the individual contents of anthocyanins, flavonols, and chlorogenic acid derivatives were measured at the last sampling date (commercial harvest). At the time of harvesting, 100 cherries from each tree, cultivar, and treatment were randomly picked for determining the fruit weight. Ripening Parameters. Color was determined in each cheek of 20 fruits from each replicate by using a Minolta colorimeter (CRC200, Minolta Camera Co., Japan), using the CIELab coordinates and expressed as a*/b* index. Fruit firmness was determined independently in 20 fruits of each replicate using a TX-XT2i texture analyzer (Stable Microsystems, Godalming, UK) interfaced to a personal computer, with a flat steel plate mounted on the machine. For each fruit, the cheek diameter was measured, and then a force that achieved a 3% deformation of the fruit diameter was applied. Results were expressed as the force−deformation ratio (N mm−1) and were the mean ± SE. After that, the 20 fruits of each sample were cut in small pieces to obtain a homogeneous sample for each replicate. TSS were determined in duplicate in the juice obtained from 5 g of each sample with a digital refractometer Atago PR-101 (Atago Co. Ltd., Tokyo, Japan) at 20 °C and expressed as grams per 100 g (mean ± SE). Total acidity (TA) was determined in duplicate in the same juice by automatic titration (785 DMP Titrino, Metrohm) with 0.1 N NaOH up to pH 8.1, using 1 mL of diluted juice in 25 mL of distilled H2O, and results (mean ± SE) were expressed as grams of malic acid equivalent per 100 g of fresh weight. Total Antioxidant Activity (TAA) Determination. TAA was quantified in duplicate in each sample as previously described.10 Briefly, 5 g was homogenized in 5 mL of 50 mM sodium phosphate buffer, pH 7.8, and 3 mL of ethyl acetate and then centrifuged at 3433

dx.doi.org/10.1021/jf500224g | J. Agric. Food Chem. 2014, 62, 3432−3437


Article

Table 1. Quality Parameters of ‘Sweet Heart’ and ‘Sweet Late’ Sweet Cherry Cultivars at Harvest As Affected by Oxalic Acid (OA) Treatmentsa

a

cultivar

control

OA (0.5 mM)

fruit weight (g)

‘Sweet Heart’ ‘Sweet Late’

6.77 ± 0.13 a 6.62 ± 0.14 a

7.73 ± 0.25 b 7.89 ± 0.15 b

7.94 ± 0.24 b 8.14 ± 0.26 b

OA (1.0 mM)

8.02 ± 0.12 bc 8.64 ± 0.32 c

OA (2.0 mM)

firmness (N mm−1)


3.09 ± 0.09 a 2.61 ± 0.09 a

3.44 ± 0.09 b 2.84 ± 0.10 b

3.66 ± 0.11 c 2.96 ± 0.10 b

3.70 ± 0.11 c 3.54 ± 0.07 c

color (a*/b*)


2.82 ± 0.09 a 3.19 ± 0.11 a

3.02 ± 0.07 b 3.44 ± 0.10 b

3.10 ± 0.12 b 3.34 ± 0.16 b

3.21 ± 0.10 bc 3.46 ± 0.14 b

TSS (g 100 g−1)


19.95 ± 0.09 a 19.05 ± 0.20 a

19.40 ± 0.11 a 19.43 ± 0.21 a

20.75 ± 0.35 b 19.60 ± 0.12 ab

20.88 ± 0.08 b 19.88 ± 0.18 ba

TA (g 100 g−1)


1.50 ± 0.01 a 1.35 ± 0.01 a

1.59 ± 0.05 b 1.41 ± 0.04 b

1.63 ± 0.02 b 1.42 ± 0.02 b

1.59 ± 0.04 b 1.54 ± 0.02 c

Data are the mean ± SE. Different letters within a row show significant differences at p < 0.05.

Hydroxycinnamic derivatives, p-coumaroylquinic acid, and hydroxybenzoic acid were characterized by chromatographic comparison according to previous reports based on retention time and UV−vis spectra.20 Anthocyanin standards (cyanidin 3-glucoside, cyanidin 3rutinoside, and pelargonidin 3-rutinoside) were purchased from Polyphenols SA (Sandnes, Norway). Anthocyanins were quantified as cyanidin 3-O-glucoside at 520 nm, cinnamic acids as 5-Ocaffeoylquinic acid at 320 nm, and flavonols as quercetin 3-Orutinoside at 360 nm and expressed as milligrams per 100 g of fresh weight (mean ± SE). Statistical Analysis. Data for the analytical determinations were subjected to analysis of variance (ANOVA). Sources of variation were days after full blossom and treatment or just treatment for individual anthocyanins, flavonols, and chlorogenic acid derivatives. Mean comparisons were performed using Tukey’s HSD test to examine if differences were significant at P < 0.05. Linear regressions were performed between phenolic and anthocyanin concentrations, as well as among total phenolics and H-TAA, taking into account data from cultivars, treatments, and all sampling dates. All analyses were performed with SPSS software package v. 12.0 for Windows.

at commercial ripening stage was significantly higher in cherries from OA-treated trees than in controls, especially with the 2.0 mM dose (Table 1). In plum and sweet cherry, postharvest treatments with OA decreased softening during storage as compared to control fruits, due to reduced activities of polygalacturonase and pectin methylesterase enzymes, leading to less pectin degradation and in turn to maintenance of fruit firmness,13,19 which could be also reduced by preharvest OA treatments. In addition, the formation of oxalate-insoluble pectin could occur as a result of OA treatment, leading to a slowing of the softening process during on-tree ripening. In previous papers, it has been shown that the color parameter ratio a*/b* is a good index to describe the ripening process in sweet cherry, because it showed both a continuous increase until the last sampling date and important differences among cultivars.3 Values at harvest of a*/b* index in ‘Sweet Heart’ and ‘Sweet Late’ cultivars were significantly higher in fruits from OA-treated trees than from controls, independent of the applied OA dose, showing a deeper red color in treated fruits than in controls (Table 1). In addition, TA and TSS were also increased in cherry fruits as a consequence of OA treatments, which could be attributed to an increase of net photosynthesis in OA-treated trees, this effect being also responsible for the higher fruit size and weight of cherries from treated trees as compared with those from control ones. In this sense, it has been reported that postharvest OA treatment of jujube fruit increased the abundance of three photosynthesis-related proteins, RuBisCO activase, RuBisCO large subunit-binding protein subunit β, and PSII oxygen-evolving complex protein.15 Postharvest OA treatment delayed the ripening process in climacteric fruits, such as mango,12 plum,13 banana,24 and jujube fruit,15 through inhibition of ethylene production. Although sweet cherry is a nonclimacteric fruit, postharvest OA treatments have been also effective in delaying the ripening process and maintaining fruit quality during storage, as well as in pomegranate, another nonclimacteric fruit.16 However, in this experiment no effect of preharvest OA treatments was observed on the ripening process of sweet cherry, and fruits from control and treated trees were harvested on the same date. Bioactive Compounds and Total Antioxidant Activity. Because the main effect of OA treatments on improving fruit quality parameters was obtained with the 2 mM dose, the content of bioactive compounds and antioxidant activity were

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RESULTS AND DISCUSSION Sweet Cherry Growth and Ripening Parameters. Fruit growth (measured as fruit volume) increased sharply from 91 DAFB until 126 and 133 DAFB in control fruit from ‘Sweet Heart’ and ‘Sweet Late’ cultivars, respectively, the increase being lower from this time to commercial maturity stage (Figure 1). However, in cherries from OA-treated trees the increase in fruit volume continued until the last sampling date, the highest fruit volume being reached with OA treatment at 2.0 mM in both sweet cherry cultivars. The effect of OA treatments on increasing fruit growth was also evident in the final fruit weight at the last sampling date, with values of 6.77 ± 0.13 and 6.62 ± 0.14 g for control fruits of ‘Sweet Heart’ and ‘Sweet Late’ cultivars, respectively, and significantly higher in cherries from OA-treated trees, ca. 8 and 8.5 g with 2.0 mM OA for ‘Sweet Heart’ and ‘Sweet Late’, respectively (Table 1). Texture is one of the most important attributes in sweet cherry, and it is often used for quality assessment, although there are considerable genotypic differences.3 Fruit firmness decreased sharply as fruit weight increased (data not shown), which simply reflects cell enlargement during fruit growth, whereas softening in the last days of on-tree fruit ripening has been attributed to cell wall modification, mainly due to increases in β-galactosidase activity.3,23 However, fruit firmness 3434



Article

Figure 2. Total phenolics and total anthocyanins during on-tree fruit development in ‘Sweet Heart’ and ‘Sweet Late’ sweet cherry cultivars treated with oxalic acid (OA) at 2.0 mM, at 98, 112, and 126 days after full blossom. Data are the mean ± SE.

Figure 3. Individual anthocyanins and flavonols at commercial harvest in ‘Sweet Heart’ and ‘Sweet Late’ sweet cherry cultivars treated with oxalic acid (OA, 2.0 mM) at 98, 112, and 126 days after full blossom. Data are the mean ± SE. Bars with different letters show significant differences between control and treated fruits for each cultivar and individual compounds.

symptoms, whereas in sweet cherry the accumulation of anthocyanins during development on-tree is a normal process of fruit ripening.3 In addition, a close relationship was found between total phenolic and total anthocyanin concentrations (y = 0.68x − 45.3; r2 = 0.812), taking into account data for both cultivars, treatments, and sampling dates, showing that in these sweet cherry cultivars anthocyanins are the main phenolic compounds, according to previous studies in other cherry cultivars.10,27 The predominant anthocyanin in both cherry cultivars was cyanidin 3-rutinoside followed by pelargonidin 3-rutinoside and cyanidin 3-glucoside, according to previous studies in other cherry cultivars,8,10,27,28 and all of them were significantly higher in OA-treated than in control cherries at the last harvest sampling date (Figure 3). The individual flavonols were found at low concentrations, the main of them being myricetin 3rutinoside in both sweet cherry cultivars, followed by quercetin 3-rutinoside and kaempferol 3-rutinoside, and all of them were significantly increased by OA treatment (Figure 3). Accord-

analyzed in cherries from control and 2 mM OA-treated trees. Total phenolics and anthocyanin concentrations increased sharply during the last 2 weeks of fruit ripening on-tree, although these values were higher in sweet cherries from OAtreated trees than in those from controls, for both cultivars (Figure 2). Accordingly, a significant increase in total phenolics as a consequence of postharvest OA treatment was also found during cold storage in sweet cherry,19 as well as during storage at room temperature in the peel of banana25 and mango26 fruits, which was related to induced resistance against pathogenic attack. However, the mechanism behind how the OA treatment affects the phenolic content at molecular levels is still not completely known and deserves further research. On the contrary, in ‘Damili’ plum, postharvest OA treatment delayed the increase of anthocyanin content that occurred in control fruits during storage, attributed to a lower activity of phenylalanine ammonia-lyase (PAL), the key enzyme involved in the biosynthesis of anthocyanins.13 However, in this fruit, the flesh reddening is associated with senescence and chilling injury 3435



Article

ingly, the main chlorogenic acid derivatives, neochlorogenic acid and chlorogenic acid, were also increased by OA treatment, whereas hydroxycinnamic derivative, p-coumaroylquinic acid, hydroxybenzoic acid, caffeic acid, and ferulic acid were found at low concentrations, without significant differences between cherries from control and treated trees (Figure 4). The

TAA was measured in hydrophilic (H-TAA) and lipophilic (L-TAA) fractions separately, because early reports demonstrated that the contribution of L-TAA was about 20−30% of the TAA in a wide range of sweet cherry cultivars.3 In ‘Sweet Heart’ and ‘Sweet Late’ cultivars H-TAA and L-TAA increased during fruit ripening on-tree, although the levels were significantly higher in fruits from OA-treated trees than in controls, especially for H-TAA (Figure 5). High correlation was found between total phenolic and H-TAA (y = 2.16x − 95.9; r2 = 0.687), which is in agreement with previous papers reporting that phenolic compounds are the main hydrophilic compounds responsible for the antioxidant capacity of sweet cherry2,3,10 and its health beneficial effects, such as the inhibition of human cancer cell proliferation.31 Nevertheless, ascorbic acid is another hydrophilic compound that can also contribute to this antioxidant activity.7 Accordingly, antioxidant activity due to phenolic compounds increased in banana peel as a consequence of postharvest OA treatment.25 In addition, postharvest OA treatment of peach14 and mango18 fruits increased activities of the antioxidant enzymes superoxide dismutase, catalase, peroxidase, ascorbate peroxidase, and polyphenol oxidase. These antioxidant enzymes, together with the antioxidant compounds (phenolics, carotenoids, and ascorbic acid), are involved in scavenging free radicals and reactive oxygen species, which are generated during ripening and senescence.30 Thus, preharvest OA treatment could also increase the antioxidant ability against oxidative damage and account for the beneficial effect of reducing cherry quality deterioration during postharvest storage. In summary, results show for the first time that the application of the natural compound OA as preharvest treatment increased fruit size and other parameters related to sweet cherry fruit quality, such as firmness and color, but did not affect the normal ripening process on-tree. In addition, at harvest the content of bioactive phenolics, including anthocyanins, flavonols, and chlorogenic acid derivatives, and H-TAA and L-TAA were significantly higher in fruits from treated trees than in control fruits. Thus, OA preharvest treatment could be a natural and useful tool to improve the

Figure 4. Individual phenolic acid derivatives at commercial harvest in ‘Sweet Heart’ and ‘Sweet Late’ sweet cherry cultivars treated with oxalic acid (OA, 2.0 mM) at 98, 112, and 126 days after full blossom. Data are the mean ± SE. Bars with different letters show significant differences between control and treated fruits for each cultivar and individual compounds.

flavonols and phenolic acid profile found in these cherry cultivars differed from previous results for other ones. Thus, for instance, in ‘Lapins’, ‘Burlat’, and ‘Sylvia’ cultivars p-coumaric acid derivatives were the main phenolic acids, together with chlorogenic and neochlorogenic acids,2 and quercetin 3rutinoside was the main flavonol in the ‘Lapins’ cultivar, which also varied depending on the cherry rootstock.29

Figure 5. Changes in hydrophilic (H-TAA) and lipophilic total antioxidant activity (L-TAA) during on-tree fruit development in sweet cherry ‘Sweet Heart’ and ‘Sweet Late’ sweet cherry cultivars treated with oxalic acid (OA, 2.0 mM) at 98, 112, and 126 days after full blossom. Data are the mean ± SE. 3436



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(13) Wu, F.; Zhang, D.; Zhang, H.; Jiang, G.; Su, X.; Qu, H.; Jiang, Y.; Duan, X. Physiological and biochemical response of harvested plum fruit to oxalic acid during ripening or shelf-life. Food Res. Int. 2011, 44, 1299−1305. (14) Zheng, X.; Tian, S.; Meng, X.; Li, B. Physiological and biochemical response in peach fruit to oxalic acid treatment during storage at room temperature. Food Chem. 2007, 104, 156−162. (15) Wang, Q.; Lai, T.; Qin, G.; Tian, S. Response of jujube fruits to exogenous oxalic acid treatment based on proteomic analysis. Plant Cell Physiol. 2009, 50, 230−242. (16) Sayyari, M.; Valero, D.; Babalar, M.; Kalantari, S.; Zapata, P. J.; Serrano, M. Prestorage oxalic acid treatment maintained visual quality, bioactive compounds, and antioxidant potential of pomegranate after long-term storage at 2 °C. J. Agric. Food Chem. 2010, 58, 6804−6808. (17) Zheng, X.; Tian, S. Effect of oxalic acid on control of postharvest browning of litchi fruit. Food Chem. 2006, 96, 519−523. (18) Ding, Z. S.; Tian, S. P.; Zheng, X. L.; Zhou, Z. W.; Xu, Y. Responses of reactive oxygen metabolism and quality in mango fruit to exogenous oxalic acid or salicylic acid under chilling temperature stress. Phyiol. Plant. 2007, 130, 112−121. (19) Valero, D.; Díaz-Mula, H. M.; Zapata, P. J.; Castillo, S.; Guillén, F.; Martínez-Romero, D.; Serrano, M. Postharvest treatments with salicylic acid, acetylsalicylic acid or oxalic acid delayed ripening and enhanced bioactive compounds and antioxidant capacity in sweet cherry. J. Agric. Food Chem. 2011, 59, 5483−5489. (20) Tomás-Barberán, F. A.; Gil, M. I.; Cremin, P.; Waterhouse, A. L.; Hess-Pierce, B.; Kader, A. A. HPLC-DAD-ESIMS analysis of phenolic compounds in nectarines, peaches, and plums. J. Agric. Food Chem. 2001, 49, 4748−4760. (21) García-Viguera, C.; Zafrilla, P.; Romero, F.; Abellá, P.; Artés, F.; Tomás-Barberán, F. A. Color stability of strawberry jam as affected by cultivar and storage temperature. J. Food Sci. 1999, 64, 243−247. (22) Gironés-Vilaplana, A.; Villaño, D.; Moreno, D. A.; GarcíaViguera, C. New isotonic drinks with antioxidant and biological activities from berries (Maqui, Açaı ́ and Blackthorn) and lemon juice. Int. J. Food Sci. Nutr. 2013, 64, 897−906. (23) Gerardi, C.; Blando, F.; Santino, A.; Zacheo, G. Purification and characterisation of a β-glucosidase abundantly expressed in ripe sweet cherry (Prunus avium L.) fruit. Plant Sci. 2001, 160, 795−805. (24) Huang, H.; Jing, G.; Guo, L.; Zhang, D.; Yang, B.; Duan, X.; Ashraf, M.; Jiang, Y. Effect of oxalic acid on ripening attributes of banana fruit during storage. Postharvest Biol. Technol. 2013, 84, 22−27. (25) Zheng, X.; Ye, L.; Jiang, T.; Jing, G.; Li, J. Limiting the deterioration of mango fruit during storage at room temperature by oxalate treatment. Food Chem. 2012, 130, 279−285. (26) Huang, H.; Zhu, Q.; Zhang, Z.; Yang, B.; Duan, X.; Jiang, Y. Effect of oxalic acid on antibrowning of banana (Musa spp., AAA group, cv. ‘Brazil’) fruit during storage. Sci. Hortic. 2013, 160, 208− 212. (27) Mozetiĉ, B.; Simĉiĉ, M.; Trebŝe, P. Anthocyanins and hidroxycinnamic acids of Lambert Compact cherries (Prunus avium L.) after cold storage and 1-methylcyclorpoene treatments. Food Chem. 2006, 97, 302−309. (28) Sharma, M.; Jacob, J. K.; Subramanian, J.; Paliyath, G. Hexanal and 1-MCP treatments for enhancing the shelf life and quality of sweet cherry (Prunus avium L.). Sci. Hortic. 2010, 125, 239−247. (29) Jakobek, L.; Šeruga, M.; Voća, S.; Šindrak, Z.; Dobričević, N. Flavonol and phenolic acid composition of sweet cherries (cv. Lapins) produced on six different vegetative rootstocks. Sci. Hortic. 2009, 123, 23−28. (30) Hodges, D. M.; Lester, G. E.; Munro, K. D.; Toivonen, P. M. A. Oxidative stress: importance for postharvest quality. HortScience 2004, 39, 924−929. (31) Serra, A. T.; Duarte, R. O.; Bronze, M. R.; Duarte, C. M. M. Identification of bioactive response in traditional cherries from Portugal. Food Chem. 2011, 125, 318−325.

reported health-beneficial properties of sweet cherry consumption.

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AUTHOR INFORMATION

Corresponding Author

*(M.S.) Fax: 34-96-6749678; E-mail: [email protected]. Funding

This work has been funded by the Spanish Ministry of Economy and Competitiveness through Project AGL201235402/ALI and by the European Commission with FEDER funds. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We thank Finca Toli Frutas, S.L., for permission to use their plots, for provision of the cherries, and for the technical support received.

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REFERENCES

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