Impaginato 33 Adv. Hort. Sci., 2018 32(1): 33-40 DOI: 10.13128/ahs-21323 Salicylic acid treatment of peach trees maintains nutritional quality of fruits during cold storage F. Razavi 1 (*), J. Hajilou 2, M.S. Aghdam 3 1 Department of Horticulture, Faculty of Agriculture, University of Zanjan, Zanjan, Iran. 2 Department of Horticulture, Faculty of Agriculture, University of Tabriz, Tabriz, Iran. 3 Department of Horticultural Science, Imam Khomeini International University, Qazvin, Iran. Key words: antioxidant enzymes, postharvest, Prunus persica L., total phenols. Abstract: Peach trees were treated with salicylic acid at 0 (control) and 1.5 mM at 15 days before harvest to study the impacts of salicylic acid on nutritional quality of peach fruits at harvest and during storage at 1°C for 28 days. Total phenols, flavonoids, and ascorbic acid contents were significantly higher in sali- cylic acid treated peach fruits after cold storage, leading to fruits with higher DPPH• and FRAP radicals scavenging capacity. In addition, peach fruits treated with salicylic acid exhibited higher antioxidant enzymes catalase (CAT), ascor- bate peroxidase (APX) and superoxide dismutase (SOD) activity after storage at 1°C for 2-4 week, leading to fruits with higher firmness and lower weight loss. Thus, salicylic acid treatment of peach trees could increase nutritional quality of peach fruits consumption, due to its effect on increasing antioxidant mole- cules, with additional effect on delaying the fruit postharvest senescence by increasing the ROS scavenging enzymes activity. 1. Introduction Peach (Prunus persica L.) is highly perishable climacteric stone fruit and is a rich source of ascorbic acid, carotenoids, and phenolics that are good sources of antioxidants (Tomas-Barberan et al., 2001). However, the rapid softening of fruit during storage at ambient temperature results in a short shelf-life of the commodity and reduced commercial fruit quality and consumer acceptance (Nunes, 2008). Due to its economic impact and also human health, great efforts have been done by researchers for delaying postharvest senescence of peach fruits during cold storage lead- ing to fruits with higher sensory and nutritional quality by applying postharvest treatment such as modified and controlled atmosphere stor- age, heat treatment, glycine betaine, nitric oxide, brassinolide; 1-methyl- cyclopropene, methyl jasmonate, oxalic acid and salicylic acid (Cao et al., (*) Corresponding author: razavi.farhang@znu.ac.ir Citation: RAZAVI F., HAJILOU J., AGHDAM M.S., 2018 - Salicylic acid treatment of peach trees maintains nutritional quality of fruits during cold storage. - Adv. Hort. Sci., 32(1): 33-40 Copyright: © 2018 Razavi F., Hajilou J., Aghdam M.S. This is an open access, peer reviewed article published by Firenze University Press (http://www.fupress.net/index.php/ahs/) and distribuited under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Competing Interests: The authors declare no competing interests. Received for publication 12 September 2017 Accepted for publication 8 November 2017 AHS Advances in Horticultural Science Adv. Hort. Sci., 2018 32(1): 33-40 34 2010; Liu et al., 2015; Kang et al., 2016; Gao et al., 2016; Razavi and Hajilou, 2016; Shan et al., 2016; Yu et al., 2016). Fruit ripening with oxidative fact is associated with reactive oxygen species (ROS) such as superox- ide radical (O2 -), hydrogen peroxide (H2O2) and hydroxyl radicals (OH-) accumulation leading to mem- brane deterioration, lipid peroxidation and DNA mutation and ultimately economical quality and quantity losses of fruits results from deterioration of their cellular metabolism (Halliwell and Gutteridge, 1989). For overcome to oxidative stress during ripen- ing which is crucial for delaying fruits deterioration and maintaining fruits sensory and nutritional quali- ty, fruits cells employed an antioxidant system, superoxide dismutase (SOD), catalase (CAT), and ascorbate peroxidase (APX) as enzymatic and ascor- bate and glutathione, tocopherols, phenolics, flavonoids, alkaloids and carotenoids as non-enzy- matic antioxidants (Apel and Hirt, 2004). SOD vocal- izes the first line of ROS scavenging and catalyzes the dismutation of O2 _ to H2O2. Then, H2O2 is eliminated by the actions of APX and CAT. APX dismutes H2O2 by conversion of AA to DHA (Foyer and Noctor, 2005). Due to extra ROS production and or incapable antiox- idant system activity, fruits may encounter oxidative damage during ripening leading to quality losses. Thus, delaying fruits ripening and maintaining fruits quality, due to its economic impact and also human health, can be results from effective antioxidant sys- tem activity in fruits during ripening, which is achiev- able by using of environmentally friendly technolo- gies such as salicylic acid (SA) as safe signaling mole- cule (Hodges et al., 2004; Asghari and Aghdam, 2010; Kumar et al., 2014), which have potential in delaying ripening, enhancing quality and attenuating biotic and abiotic stress of fruits (Asghari and Aghdam, 2010). According to capability of SA in using as prehar- vest treatment, Gimenez et al. (2014) reported that sweet cherry fruits treated at preharvest with SA at 0.5 mM and ASA at 1 mM exhibited higher total phe- nolics and total anthocyanins, as well as higher hydrophilic and lipophilic antioxidant activity at com- mercial harvest (Gimenez et al., 2014). Also, Gimenez et al. (2017) reported that sweet cherry fruits treated at preharvest with SA at 0.5 mM and ASA at 1 mM exhibited higher total phenolics and total antho- cyanins, as well as higher hydrophilic antioxidant activity during storage at 2°C for 28 days. Also, cherry fruits treated at preharvest with SA and ASA exhibit- ed higher antioxidant enzymes catalase (CAT), ascor- bate peroxidase (APX) and superoxide dismutase (SOD) during storage at 2°C for 28 days. Valverde et al. (2015) reported that the sweet cherry fruits treat- ed with preharvest 1 mM methyl salicylate exhibited higher total phenolics and anthocyanins content at harvest and during storage at 2°C for 28 days, leading to fruit with higher hydrophilic TAA (H-AA). Also, sweet cherry fruits treated with preharvest 1 mM methyl salicylate exhibited higher antioxidant enzymes CAT, APX and SOD activities during storage at 2°C for 28 days. Thus, salicylates treatment of sweet cherry trees enhances health boosting attrib- utes of cherry fruits consumption, by increasing antioxidant molecules, with supernumerary impacts on delaying the sweet cherry fruits postharvest senescence by enhancing ROS scavenging enzymes activities (Gimenez et al., 2017). It has been suggest- ed that the preharvest salicylates treatments would have commercial fondness with low earnings costs and with considerable profits in fruit nutritional qual- ity (Gimenez et al., 2017). Moreover, postharvest treatment of peach fruit with SA at 2 mM enhanced higher levels of POD, CAT and SOD activities during cold storage as compared with control peaches, which were accompanied by lower polyphenol oxi- dase (PPO) activity. In addition, SA treated fruits exhibited higher firmness and radical scavenging activity (Tareen et al., 2012). Then, the aim of this research was to evaluate for the first time the impacts of preharvest SA treatment of peach trees on bioactive molecules and the antiox- idant enzymes SOD, CAT, and APX activities at har- vest and during cold storage. 2. Materials and Methods Fruits and treatments The experiment was carried out on 5-year-old peach [Prunus persica (L.) Batsch ‘Anjiry maleki’] trees grafted on GF 677 rootstock, in a commercial orchard located in the north-west Iran. The trees were spaced at 6×5 m, receiving identical cultural practices and trained to an open vase system. Twelve trees were selected for uniform size and fruit load and sprayed with SA at concentrations of 1.5 mM on whole tree and control trees receiving only water. A surfactant (Tween-20) was added to each solution as a wetting agent for maximum SA absorption, and sprays were applied at 15-day before commercial harvest. Fruit from control and SA treated trees were Razavi et al. - Salicylic acid and nutritional quality of peach fruit 35 harvested at commercial maturity and immediately transported to the laboratory. The fruits were select- ed for uniform size, color and absence of mechanical damage, and then one group was analyzed 24 h after harvest and another groups stored at 1±0.5°C and 90% RH for 28 d. At 7-day intervals, 5 fruits from each of three replications were selected, and left for a further 24 h at 20°C (shelf-life), and subjected to physicochemical analysis. Flesh firmness and weight loss At each sampling date, flesh firmness (N) was measured on the opposite sides of the fruit after peel removal using an Effegi penetrometer (Model FT 011) equipped with an 8 mm diameter probe. To determine the weight loss, five fruits for each repli- cates were weighed at harvest and at 7 day intervals during cold storage. Results were expressed as per- centage of weight loss relative to the initial fruit weight. Antioxidant enzymes activity assays Crude extract for APX enzymes was performed by homogenizing 1 g of frozen fruits tissue with 5 mL of phosphate buffer 100 mM, pH= 7.8 containing 1% (w/v) PVP, 1 mM EDTA and 5 mM ascorbic acid. The homogenate was centrifuged at 18,000 g for 10 min at 4°C and the supernatant used for enzyme assay. APX activity was determined by the method of Nakano and Asada (1987) with some modification. The reaction mixture consisted of 3 mL of 50 mM potassium phosphate, pH 7.0, 0.2 mM ascorbic acid, 0.2 mM EDTA and 0.5 mL of crude extract, and the reaction was allowed to start by adding 0.5 mL of 0.5 mM H2O2. The decrease in absorbance at 290 nm was recorded spectrophotometrically for 3 min and APX activity expressed as U mg protein-1. Crude extract for CAT and SOD enzymes was per- formed by homogenizing 1 g of frozen fruits tissue with 3 mL of phosphate buffer 50 mM, pH= 7.8 con- taining 2% (w/v) PVP, 1 mM EDTA. The homogenate was centrifuged at 14,000 g for 20 min at 4°C and the resulting supernatant was used for enzyme assay. CAT activity was quantified following the method described by Zhang et al. (2013). The reaction mix- ture consisted of 50 mM phosphate buffer (pH 7), 15 mM H2O2 and 0.1 mL of crude extract in a final vol- ume of 3 mL. Decreases in absorbance at 240 nm at intervals of 30 s were recorded spectrophotometri- cally. CAT activity expressed as U mg protein-1. SOD activity was assayed according to the method described by Zhang et al. (2013). One unit of SOD activity was defined as the amount of enzyme that causes a 50% inhibition of nitro blue tetrazolium reduction under assay conditions and the results were expressed as U mg protein-1. Total protein con- tent in the enzyme extract was assayed according to the method described by Bradford (1976). Total phenolics, flavonoids and ascorbic acid contents The amount of total phenolics in extracts was determined according to the Folin-Ciocalteu reagent method (Singleton and Rossi, 1965). Gallic acid was used as a reference standard, and the total phenolic contents of extract were expressed as mg gallic acid equivalent 100 g-1 fresh weight (FW). Total flavonoids content was determined in accordance with a proto- col described by Kaijv et al. (2006). A calibration curve was obtained using quercetin as a standard, and the results were expressed as µmol quercetin equivalent (QE) 100 g-1 FW. Ascorbic acid content in the fruits was measured by 2,6-dichlorophenol indophenol dye method (AOAC, 1984). For each sam- ple, 10 g fresh fruits pulp was homogenized with 3% metaphosphoric acid solution and the mixture was made up to 100 mL. An aliquot of 10 ml was then titrated against the dye (2,6-dichlorophenol indophe- nol) till the pink color appeared. Ascorbic acid con- tent was estimated from a calibration curve of L- ascorbic acid and results expressed as mg ascorbic acid equivalents 100 g-1 FW. Total antioxidant activity The FRAP assay was carried out using TPTZ (2,4,6- tripyridyl-Striazine) solution according to the proce- dure described by Benzie and Strain (1999). FRAP reagent was prepared freshly by mixing 2.5 ml of solutions TPTZ (10 mM, dissolved in 40 mM HCl) and FeCl3 (20 mM) in 25 ml of acetate buffer (300 mM concentration and 3.6 pH). A 50 μL of the diluted sample was added to 1.5 mL of FRAP reagent. The absorbance of the mixture was measured at 593 nm after 4 min. incubation at 37°C using a UV-visible spectrophotometer (T-60, PG Instrument UK). A cali- bration curve was built using a standard solution of FeSO4 and the FRAP values of extract were expressed as mmol Fe(II)/g fresh weight. The method of Dehghan and Khoshkam (2012) was used for measuring the DPPH radical scavenging ability of peach extracts. The amount of 50 μL of peach extract was allowed to react with 1.95 mL of DPPH radical solution (0.1 mM in methanol) for 30 min. The decrease in absorbance from the resulting solution (AS) was monitored at 517 nm in a UV-visi- ble spectrophotometer (T-60, PG Instrument UK). Absorbance of the blank solution of DPPH (2 ml) was Adv. Hort. Sci., 2018 32(1): 33-40 36 used as an experimental control (AC). The radical scavenging activity (RSA %) of the peach fruits extracts was calculated according to the following formula: RSA % = 100 (Ac-As) Ac Statistical analysis The experiment was performed using a factorial design with SA treatment and storage time as the two factors. Differences among means of data were analyzed by Duncan’s test at p≤0.05 (n=3). All statisti- cal analyses were performed with SPSS version 20.0. 3. Results and Discussion As shown in figure 1, fruits weight loss increased and fruits firmness decreased during cold storage in control and treated fruits, but fruits weight loss was significantly lower (P<0.05) and fruits firmness were significantly higher (P<0.05) after storage at 1°C for 2-4 weeks in peach fruits coming from SA treated trees than in controls (Fig. 2). Cell wall degradation by cell wall hydrolases such as polygalactosidase (PG), pectin methyl esterase (PME), β-galactosidase (β-Gal) and xylanase along with cell membrane dete- rioration led to fruits softening that are associated with climacteric rise in ethylene production (Srivastava and Dwivedi, 2000). Zhang et al. (2003) reported that kiwifruit treated with acetyl salicylic acid exhibited lower ethylene biosynthesis during fruit ripening, results from lower ACC oxidase (ACO) and ACC synthase (ACS) activity. Kiwifruits during postharvest softening of at 20°C exhibited lower endogenous SA content, which was concurrent with higher LOX activity and higher ethylene production. LOX by generation of O2 - have a regulatory role in ethylene biosynthesis via a contribution in ACC con- version to ethylene (Xu et al., 2000). Kiwifruit treated with acetyl salicylic acid exhibited higher endogenous SA accumulation associated with lower LOX activity, O2 - accumulation, and ACS and ACO activities and eventually delayed ethylene biosynthesis. Zhang et al. (2003) suggested that the higher fruits endoge- nous SA accumulation leads to lower ethylene biosynthesis and higher firmness. Also, Srivastava and Dwivedi (2000) reported that SA treatment delayed banana fruits ripening, results from lower ethylene biosynthesis due to lower ACS and ACO enzymes activity. They also reported that SA treat- ment maintains fruits firmness, results from lower PG, xylanase and cellulase activity. Maintaining firm- ness in peach fruits treated with SA may be result of directly inhibition of cell wall degradation enzymes activity, indirectly decreasing ethylene production, and also higher firmness in peach fruit treated with SA could be attributed to endogenous SA accumula- tion which lead to lower LOX activity and ROS accu- mulation. Loss of weight in stored peach is mainly due to evaporation of water from the fruits and becomes apparent as shriveling. The lower weight loss in peach fruits treated with SA could be attrib- uted to stabilization of cell membrane as well as cell wall integrity and the permeability of tissues. Maintaining ascorbic acid content in fruits during postharvest ripening is crucial for human health, due to antioxidant function of ascorbic acid and also for human disability for ascorbic acid synthesis (Davey et al., 2000; Hassanpour et al., 2011). As shown in fig- ure 3, ascorbic acid content decreased in control and treated fruits during storage at 1°C for 28 days, but ascorbic acid content was significantly higher during cold storage in SA treated peach fruits than in con- trols (P<0.05) (Fig. 3). Huang et al. (2008) reported Fig. 2 - Firmness of peach fruits treated with preharvest SA at 1.5 mM stored at 1±0.5°C for up to 28 days. Data shown are mean ± standard deviation of three replicate (n = 3). Fig. 1 - Weight loss of peach fruits treated with preharvest SA at 1.5 mM stored at 1 ± 0.5°C for up to 28 days. Data shown are mean ± standard deviation of three replicate (n = 3). Razavi et al. - Salicylic acid and nutritional quality of peach fruit 37 that navel orange fruit treated with SA exhibited higher ascorbic acid content, results from increasing cytosolic Ca+2, enhancing GR enzyme activity, which in turn could increase GR/APX system activity leading to higher ascorbate/dehydroascorbate (AA/DHA) and glutathione/glutathione disulfide (GSH/GSSG) ratios. Also, Rao et al. (2011) reported that the sweet pep- per treated with SA and CaCl2 exhibited higher ascor- bic acid content, which results from lower ascorbic acid oxidase (AAO) enzyme activity. Higher AA con- tent in peach fruits treated with SA may be attrib- uted to higher GR/APX system activity due to increase of cytosolic Ca+2 concentrations and or lower AAO enzyme activity. Enhancing phenols accumulation in fruits during postharvest ripening is crucial not only due to their contribution in nutritional quality attributes of fruits such as color, astringency, bitterness and flavor, but also phenols are superior antioxidants and display ROS scavenging activity (Hassanpour et al., 2011). Due to phenols ROS scavenging capacity and their function in decreasing low-density lipoproteins (LDL), consumption of fruits with higher phenols would be associated with lowered risk of heart disease (Vinson et al., 2001). As shown in figure 4 and 5, total phe- nols and flavonoids contents were significantly higher after storage at 1°C for 2-4 week in SA treated peach fruits than in controls (P<0.05). It has been reported that sweet cherry fruits treated at preharvest with SA at 0.5 mM and ASA at 1 mM exhibited higher total phenolics and total antho- cyanins, as well as higher total antioxidant activity at commercial harvest (Gimenez et al., 2014) and during storage at 2°C for 28 days (Gimenez et al., 2017). Also, Valverde et al. (2015) reported that the total phenolics and anthocyanins content were significant- ly higher in methyl salicylate treated sweet cherry fruits at harvest and during storage at 2°C for 28 days, leading to fruits with higher hydrophilic TAA (H- AA). Due to higher PAL enzyme activity in cornelian cherry fruits treated with SA and CaCl2, which was associated with higher total phenols, flavonoids and anthocyanins accumulation (Aghdam et al., 2013; Dokhanieh et al., 2013), it can be postulated that the higher total phenols and flavonoids contents in SA treated peach fruits may attributed to higher PAL activity. Wang et al. (2015) reported that the apricot fruits treated with SA exhibited higher total phenols and flavonoids accumulation and higher hydrophilic antioxidant capacity. Higher hydrophilic antioxidant capacity in apricot fruits treated with SA was associ- ated with higher PAL enzyme activity. Also, apricot fruits treated with SA exhibited higher SOD enzyme activity and lower CAT and APX enzymes activity, which leads to lower O2 - and higher H2O2 accumula- tion. H2O2 as second messenger can activate PAL enzyme activity, as a key enzyme in phenyl- propanoids pathway, and ultimately higher total phe- Fig. 4 - Total flavonoids content of peach fruits treated with preharvest SA at 1.5 mM stored at 1±0.5°C for up to 28 days. Data shown are mean ± standard deviation of three replicate (n = 3). Fig. 5 - Total phenolics content of peach fruits treated with preharvest SA at 1.5 mM stored at 1±0.5°C for up to 28 days. Data shown are mean ± standard deviation of three replicate (n = 3). Fig. 3 - Ascorbic acid content of peach fruits treated with preharvest SA at 1.5 mM stored at 1±0.5°C for up to 28 days. Data shown are mean ± standard deviation of three replicate (n = 3). Adv. Hort. Sci., 2018 32(1): 33-40 38 nols and flavonoids accumulation (Wang et al., 2015). Since peach fruits treated with SA exhibited higher CAT and APX enzymes activity, higher total phenols and flavonoids contents cannot be attributed to high- er H2O2 accumulation. As shown in figure 6 and 7, DPPH and FRAP scav- enging capacity of the peach fruits treated with SA were significantly enhanced during storage at 1°C for 28 days (P<0.05), showing that SA treatment stimu- lated the scavenging capacity of the peach fruits on DPPH and FRAP radicals, which may be results from higher total phenols and flavonoids accumulation (Razavi and Hajilou, 2016). Dokhanieh et al. (2013) and Aghdam et al. (2013) reported that the cornelian cherry fruits treated with SA and CaCl2 exhibited higher total phenols, flavonoids, and anthocyanins accumulation results from higher PAL enzyme activity as key enzyme in phenylpropanoid pathway which is responsible for antioxidant molecules biosynthesis. We proposed that SA treatment may stimulate the accumulation of phenol, and flavonoid in the peach fruits by activating phenylpropanoid pathway. Higher DPPH and FRAP scavenging capacity of the peach fruits treated with SA may be results from higher total phenols and flavonoids accumulation due to higher PAL enzyme activity concurrent with higher ascorbic acid accumulation due to higher cytosolic Ca2+ and or lower AAO enzyme activity. As shown in figure 8, 9 and 10, antioxidant enzymes CAT, SOD and APX activity increased during storage at 1°C for 28 days in control and treated fruits, and SOD and APX activities were significantly higher during all the storage period at 1°C for 28 days in SA treated peach fruits than in controls (P<0.05), while concerning CAT, higher activity was observed only after 3-4 weeks of storage. Valverde et al. (2015) reported that sweet cherry fruits treated at preharvest with methyl salicylate exhibited higher antioxidant enzymes CAT, APX and SOD during stor- age at 2°C for 28 days. Gimenez et al. (2017) report- ed that sweet cherry fruits treated at preharvest with SA at 0.5 mM and ASA at 1 mM exhibited higher antioxidant enzymes CAT, APX and SOD during stor- age at 2°C for 28 days. Thus, salicylates treatment of peach trees enhances health boosting attributes of peach fruits consumption, by increasing antioxidant Fig. 8 - CAT activity of peach fruits treated with preharvest SA at 1.5 mM stored at 1±0.5°C for up to 28 days. Data shown are mean ± standard deviation of three replicate (n = 3). Fig. 9 - SOD activity of peach fruits treated with preharvest SA at 1.5 mM stored at 1±0.5°C for up to 28 days. Data shown are mean ± standard deviation of three replicate (n = 3). Fig. 6 - DPPH scavenging capacity of peach fruits treated with preharvest SA at 1.5 mM stored at 1 ± 0.5°C for up to 28 days. Data shown are mean±standard deviation of three replicate (n = 3). Fig. 7 - FRAP scavenging capacity of peach fruits treated with preharvest SA at 1.5 mM stored at 1±0.5°C for up to 28 days. Data shown are mean ± standard deviation of three replicate (n = 3). Razavi et al. - Salicylic acid and nutritional quality of peach fruit 39 molecules, with supernumerary impacts on delaying the peach fruits postharvest senescence by enhanc- ing ROS scavenging enzymes activities. Higher antiox- idant enzymes activity, together with higher antioxi- dants molecules accumulation, in peach fruits during storage, as a results of preharvest SA treatment, could contribute to ROS scavenging during the postharvest ripening, which in turn, leads to delaying peach fruits postharvest ripening and senescence. SA enhance antioxidant systems activity by avoiding and/or scavenging ROS, which led to decrease oxida- tive stress during peach fruits ripening and ultimately maintain postharvest quality by prevention of adverse effects of ROS on fruits quality. 4. Conclusions SA, as safe signaling molecule, could enhance nutritional quality and improve health promoting attributes of peach fruits consumption. 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