Efficacy of Postharvest Diphenylamine Treatment on Reducing Oleocellosis in Valencia Orange Fruits

LIU Li-dan1,2,WU Ri-zhang1,ZENG Kai-fang1,3,*

(1. College of Food Science, Southwest University, Chongqing 400715, China;2. The Industrialization of Agriculture Office in Tongren, Tongren 554300, China;3. Laboratory of Quality and Safety Risk Assessment for Agro-products on Storage and Presevation (Chongqing), Ministry of Agriculture, Chongqing 400715, China)

 

Abstract:Our goal in this study was to evaluate the efficacy of diphenylamine (DPA) treatment on reducing oleocellosis in Valencia orange fruits (Citrus sinensis L. Osbeck) and its mechanism. The results showed that 7 mmol/L DPA treatment was significantly effective to control oleocellosis in Valencia orange fruits, which could enhance the activities of antioxidant enzymes including superoxide dismutase (SOD), catalase (CAT), peroxidase (POD), ascorbate peroxidase (APX) and glutathione reductase (GR) and the contents of antioxidant compounds. In addition, there was a decline in polyphenoloxidase (PPO) activity in DPA-treated fruits during the later period of storage. These results indicated DPA treatment could alleviate the symptoms of oleocellosis in Valencia orange fruits by regulating malondialdehyde (MDA) level and antioxidant enzyme activity.

Key words:Valencia orange fruit;oleocellosis;diphenylamine;antioxidant

采后二苯胺处理减轻夏橙果实油胞病的作用

刘丽丹1,2,吴日章1,曾凯芳1,3,*

(1.西南大学食品科学学院,重庆 400715;2.贵州省铜仁市农业产业化办公室,贵州 铜仁 554300;

3.农业部农产品贮藏保鲜质量安全风险评估实验室(重庆),重庆 400715)

 

摘 要:研究通过二苯胺处理减轻夏橙果实油胞病的效果及其机制。结果表明:7mmol/L二苯胺处理对夏橙果实油胞病的控制具有显著效果,二苯胺处理提高了夏橙果实中相关抗氧化酶如超氧化物歧化酶(SOD)、过氧化氢酶(CAT)、过氧化物酶(POD)、抗坏血酸酶(APX)和谷胱甘肽还原酶(GR)的活性和抗氧化物质的含量。另外,二苯胺处理后的果实在贮藏后期多酚氧化酶(PPO)活性显著低于对照果实。因此,二苯胺处理可通过调节丙二醛(MDA)水平、抗氧化相关酶活性以及PPO活性来减轻夏橙果实的油胞病症状。

关键词:夏橙;油胞病;二苯胺;抗氧化

中图分类号:TS255.3;S666.4 文献标志码:A 文章编号:1002-6630(2013)24-0273-06

doi:10.7506/spkx1002-6630-201324057

Oleocellosis, a common physiological rind disorder of citrus fruit, is caused by many factors, such as mechanical damage, storage conditions[1-2]. It is characterized by sunken areas on flavedo and collapsed oil glands, which starts between the damaged epidermis and the collapsed layers of flavedo, eventually spread and affect oil glands, then followed by brown spot with different size and shape on citrus peel[1,3-4]. Thus, the damaged peel shows dark and color fading in mature fruit[4], which could decrease the commercial value of citrus.

Several postharvest treatments have been developed to control oleocellosis on citrus peel. Ben-Yehoshua et al.[5] reported that Noxan on ‘Shamout’ oranges was decreased by changing packaging condition. Meanwhile, postharvest rind disorders in citrus fruit were reduced by modified atmosphere packaging[6]. Previous study showed that exogenous ethylene treatment was also effective for reducing oleocellosis on citrus rind, which improved the production of endogenous abscisic acid content[7]. Additionally, Alférez et al.[2] found that low relative humidity (RH) storage condition had an induction on ethylene content, resulting in oleocellosis on citrus rind. However, it was still necessary to continue searching for effective measures to control oleocellosis on citrus rind.

According to Wild[8] and Knight[1] et al., the oleocellosis on citrus rind has a close correlation with the release of phytotoxic oil from oil glands within the rind. Exogenous oil application had a direct effect on damaging cell structure, leaving notable spots on citrus rind. Moreover, physiological disorder on citrus rind might be caused by reactive oxygen species (ROS) accumulation, which was produced by cell lipid membrane per-oxidation due to damaged cell structure[4,9]. Diphenylamine (DPA) was an antioxidant which was generally used to control postharvest superficial scald of apple[10]. Meanwhile, Purvis[11] found that DPA could enhance the chilling tolerance of pepper fruit. However, to our knowledge, there was no report about the effect of DPA on oleocellosis. At present time, heat treatment is one of the most easily applied and environmentally safe fruit treatments, in the form of hot water dips, hot dry air, or vapor heat[12] which was effective for controlling cold damage on citrus. In addition, Ghasemnezhad et al.[13] found that postharvest heat treatment could induce fruit tolerance to cold temperatures and produce physiological changes in the rind and changes in antioxidants ability. The objective of this work was to investigate whether oleocellsis on Valencia orange fruit could be controlled by DPA treatment, and the effect of DPA on the malondialdehyde (MDA) content, antioxidant and enzyme activities of Valencia orange fruit peel stored at a non-chilling temperature.

1 Materials and Methods

1.1 Fruit materials

Fruits of Valencia orange (Citrus sinensis L. Osbeck) at the commercially mature stage were harvested from the same location and block on may 26, 2011 from a commercial orchard in Chongqing. Fruits selected were uniform in shape, colour, size, and free from blemishes and dieseases.

1.2 DPA treatments

For the DPA treatment, Valencia orange fruit were dipped in diphenylamine (DPA) with concentrations of 1, 3, 5 mmol/L and 7 mmol/L for 3 min and air-dried. For the DPA with hot water (HW) treatment, Valencia oranges were submerged in circulating water at 45 ℃ for 4 min. Then, the fruits were dipped in diphenylamine (DPA) at 7 mmol/L for 3 min and then air-dried. For the control, Valencia oranges were dipped in distilled water for 3 min.

Following treatments, according to Wild[8], absorbent 6 mm cardboard discs (Whatman Antibiotic Assay discs) was placed on 18 mm wide transparent adhesive tape. Commercially pure orange rind oil (Skinhelp Biotech. Ltd., Plymouth, England, 15 µL) was pipetted onto a disc, which was placed on the adhesive tape, then placed on the fruits. The oranges were packaged individually in plastic bags and held for 3 days at 5 ℃, RH 85%-90%. The tapes were then removed. Later, all fruits were individually packaged in plastic bags and stored at 5 ℃, RH 85%-90%.

For the enzymes, Total phenols, ascorbic acid (AsA) and glutathione (GSH) concentrations assay, fruit samples for control, 7 mmol/L DPA treatment were obtained from fruits peel at various time intervals (0, 3, 6, 9 d and 12 d) after treatment.

In all experiments, each treatment involved eight fruits, with three replicates arranged in a completely randomized design. The experiment was conducted twice with similar results.

1.3 Visual assessment

According to the method of Knight et al.[1], blemish severity was assessed using a scoring system. Rind collapse and discoloration were assessed using two separate subjective scales. For peel collapse, the scale was: 0 (nil), 1 (very slight), 2 (slight), 3 (medium), 4 (high). Discoloration was scored as: 0 (nil), 1 (very slight), 2 (slight), 3 (medium), 4 (high) and 5 (extreme). Collapse score =Σ (collapse level ×number of citrus with rind disorder relative to the total value)/ total fruit number. Discoloration =Σ (discoloration level ×number of citrus with rind disorder relative to the total value)/ total fruit number.

1.4 MDA, GSH, AsA and total phenols content

MDA content was determined by the thiobarbituric acid (TBA) reaction according to Hodges et al.[14]. The MDA concentration was expressed in nmol/g fruit weight (mf).

GSH content was measured according to a method described by Brehe et al.[15]. 0.5 mL aliquots of the supernatant were thoroughly mixed with 2 mL of 0.1 mol/L phosphate buffer (pH 7.7) and 0.5 mL of 4 mmol/L 5,5-dithiobis-2-nitrobenzoic acid. The reaction was held at 25 ℃ for 10 min. The absorbance of the supernatant at 412 nm was measured using a spectrophotometer. The GSH content was expressed in μmol/g mf.

AsA content was determined according to a method described by El-Bulk et al.[16]. Two grams of frozen pericarp tissues were homogenized with small amount of 2% oxalic acid in a cooled mortar. Then the homogenate was diluted to 50 mL and filtered. The AsA content was expressed as mg/100 g mf.

The level of phenolic compounds was measured according to the method of Pirie et al.[17]. One gram of flesh tissue was homogenized with 6 mL ice-cold 1% HCl-methanol solution and then centrifuged at 15000×g for 15 min at 4 ℃. The total phenol content was expressed in OD280nm/g mf.

1.5 Enzyme activities

To extract superoxide dismutase (SOD), 2.0 g of frozen pericarp tissues were homogenized with 6 mL of 50 mmol/L cold phosphate buffer (pH 7.8) containing 5 g/100 mL polyvinylpyrrolidone and 5 mmol/L dithiothreitol in a cooled mortar. The homogenate was centrifuged at 12000×g for 30 min at 4 ℃. SOD activity was measured by the decrease in optical density of nitro-blue tetrazolium (NBT) dye by the enzyme according to the method of Prochazkova et al.[18]. One unit of activity was defined as the amount of enzyme that would inhibit 50% of NBT photoreduction at 560 nm.

To extract antioxidant enzymes, 2.0 g of frozen pericarp tissues were homogenized with 6 mL of 0.1 mol/L cold phosphate buffer (pH 6.8) containing 0.2 g polyvinyl-pyrrolidone in a cooled mortar. The homogenate was centrifuged at 12000×g for 15 min at 4 ℃. The supernatant was subsequently used for assays of peroxidase (POD) activity. POD activity was assayed according to Srivastava et al.[19]. Changes in the absorbance of the reaction solution at 470 nm were determined every 15 s. One unit of activity was defined as the amount of enzyme required to increase 1 absorbance unit in the optical density at 470 nm/min and expressed in U/g mf. The polyphenoloxidase (PPO) was assayed according to Zauberman et al.[20]. The reaction solution (3 mL) for PPO activity contains 2.0 mL of 0.1 mol/L phosphate buffer (pH 6.8), 0.9 mL of 25 mmol/L brenzcatechin and 0.1 mL of enzyme extract. Changes in the absorbance of the reaction solution at 420 nm were determined every 15 s. One unit of activity was defined as the amount of enzyme required to increase 0.01 absorbance unit in the optical density at 420 nm/min and expressed as U/g mf.

To extract antioxidant enzymes, 2.0 g of frozen pericarp tissues were homogenized with 6 mL of 50 mmol/L cold phosphate buffer (pH 7.5) containing 2 g/100 mL polyvinyl-pyrrolidone and 5 mmol/L dithiothreitol in a cooled mortar. The homogenate was centrifuged at 12000 × g for 30 min at 4 ℃. The supernatant was subsequently used for assays of catalase (CAT), ascorbate peroxidase (APX) and glutathione reductase (GR) activity.

CAT activity was assayed according to Havir et al.[21]. Changes in the absorbance of the reaction solution at 240 nm were read every 30 s. One unit of activity was defined as the amount of enzyme required to decrease 0.01 absorbance unit in the optical density at 240 nm/min and expressed in U/g mf. APX activity was measured according to Nakano et al.[22]. The assay depends on the decrease in absorbance at 290 nm as ascorbate was oxidized. One unit of activity was defined as the amount of enzyme required to decrease 0.01 absorbance unit in the optical density at 290 nm/min and expressed in U/g mf. GR was measured according to Foyer et al.[23]. One unit of activity was defined as the amount of enzyme required to decrease 0.01 absorbance unit in the optical density at 340 nm/min and expressed in U/g mf.

1.6 Statistical analysis

All Statistical analyses were performed using SPSS 11.0 software. Mean separations were performed by employing Duncans multiple comparison. Each experiment had three replicates and all experiments were repeated at least twice.

2 Results and Analysis

2.1 Effect of DPA and DPA+HW treatment on rind collapse and discoloration score of Valencia orange fruit

440089.jpg 

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Fig.1 Effect of DPA and DPA combined with HW treatment on rind collapse (A) and discoloration (B) scores of Valencia orange fruits

In Fig. 1, during storage, collapse and discoloration score of DPA-treated fruit were lower than those of control. Rind collapse and discoloration score of Valencia orange fruit was significantly decreased with the increase of DPA concentration during storage. Collapse and discoloration score of the 7 mmol/L DPA treated fruit were about 70.79% and 79.91% lower than those of control at 12 d. However, there was no significant difference between 7 mmol/L DPA and 7 mmol/L DPA + HW treatment before 12 d (P > 0.05).

2.2 Effect of DPA treatment on MDA content, SOD, CAT and POD activities in Valencia orange fruit

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Fig.2 Effect of DPA treatment on MDA content (A), and SOD (B), CAT (C) and POD (D) activities in Valencia orange fruits

In Fig. 2A, MDA content was reduced by DPA treatment during storage. MDA content in fruit was about 28.65%, 10.84%, 18.51%, 51.78% or 70.99% lower than that of the control at 0, 3, 6, 9 d or 12 d after 7 mmol/L DPA treatment, respectively. SOD activity was enhanced by
7 mmol/L DPA treatment. SOD activity in 7 mmol/L DPA-treated fruit was about 8.11%, 3.90% or 37.16% higher than that of control at 6, 9 d or 12 d, respectively (Fig. 2B). Meanwhile, fruits treated with 7 mmol/L DPA maintained a higher level of CAT activity. CAT activity in 7 mmol/L DPA treated fruit was about 70.76%, 52.01% and 200.00% higher than that of control at 0, 9 d or 12 d storage, respectively (Fig. 2C). In Fig. 2D, POD activity was enhanced by
7 mmol/L DPA treatment at the early period of storage. POD activity in 7 mmol/L DPA-treated fruit was about 28.61%, 9.33% or 25.46% higher than that in control at 0, 3 d or 6 d, respectively.

2.3 Effect of DPA treatment on APX, GR activities and AsA, GSH contents in Valencia orange fruit

During storage, an enhancement in APX activity in DPA-treated fruit was observed (Fig. 3A). APX activity in DPA-treated fruit was about 12.16%, 30.56%, 9.06% or 11.54% higher compared with control at 0, 3, 6 d or 9 d, respectively. In Fig. 3B, GR activity had an increase during early storage, followed by a decline after 9 d. In addition, DPA-treated fruit had a higher GR activity than control during storage.

AsA content decreased gradually before 6 d, followed by a rapid increase (Fig. 3C). AsA content in DPA-treated fruit was higher than that of the control after 3 d. In Fig. 3D, there was a gradual increase in GSH content of DPA-treated fruit before 9 d, followed by a gradual decline. Moreover, GSH content in DPA-treated fruit was higher than that in control after 3 d.

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Fig.3 Effect of DPA treatment on APX (A), GR activities (B) and
AsA (C) and GSH contents (D) in Valencia orange fruits

2.4 Effect of DPA treatment on total phenols content and PPO activity in Valencia orange fruit

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Fig.4 Effect of DPA treatment on total phenols content (A) and PPO (B) activity in Valencia orange fruits

In Fig. 4A, total phenols content in fruit was decreased by 7 mmol/L DPA treatment after 6 d storage. In Fig. 4B, there was no significant difference in PPO activity among control and DPA treatment during storage except 9 d. PPO activity in DPA-treated fruit was about 61.68% lower than that in control at 9 d, respectively.

3 Discussion and Conclusion

Treating Valencia orange fruit with DPA prior to storage at low temperature inhibited the development of oleocellosis induced by oil application, just as it inhibits superficial scald in apple fruit during storage[10,24] and chilling injury of green bell pepper fruit[11]. Increasing the concentration of DPA from 1 to 7 mmol/L resulted in a higher reduction in oleocellosis on Valencia orange fruit rind. Previous study demonstrated that hot water treatment could improve chilling tolerance on grape berries[25] and delay cold-induced banana peel blackening[12]. However, 7 mmol/L DPA with hot water treatment had no significant effect on reducing the development of oleocellosis on Valencia oranges rind compared with 7 mmol/L DPA treatment (P>0.05).

Rapid generation of ROS has been considered as one of the earliest events correlated with physiological rind disorder of citrus fruit, such as chilling[9] or peel pitting[4]. ROS in plants are highly reactive and toxic, and causes damage to proteins, lipids and carbohydrates which ultimately results in oxidative stress[26]. Moreover, ROS can cause biomembrane degreasing, membrane lipid over-oxidation, making cell membrane degenerated and harmful peroxide accumulated, such as MDA[27] which is a secondary end product of polyunsaturated fatty acid oxidation. Our study showed that MDA content was rapidly decreased by DPA treatment. The study was in accordance with Zhao Ruiping et al.[28] who found that the MDA content of ‘Yali’ pears decreased suddenly after DPA treatment. Similar phenomena were also observed in relevant studies on other fruits[29-30].

Furthermore, plants have several mechanisms to prevent or alleviate the damage from ROS, since an effective enzymatic antioxidant system in plants can protect tissues from deleterious and degradative reactions by removing ROS[7,9]. SOD is the first key enzyme that can get rid of ROS and also can quickly catalyze superoxide radical into H2O2 and O2, one kind of ROS in plant, can permeate cell membrane easily and play an important role in signal transmission of resisting illness, but a large number of H2O2 can damage plant tissues, causing physiological diseases[26]. In addition, H2O2 was transformed into H2O and O2 by the CAT, POD and AsA-GR systems[9,22,31]. AsA and GSH can also serve as chemical scavengers of ROS in non-enzymatic reactions[15]. Moreover, it was reported that DPA may remove ROS as a free radical scavenger and inhibit memberane lipid per-oxidation as an antioxidant to decrease chilling index on fruits[28,32]. Our study showed that SOD, CAT and POD activities were enhanced by DPA treatment. Our study also showed that treated fruit had much higher GSH and AsA content, APX and GR activity than control after DPA treatment, which might partly account for protecting the tissues from injury of excessive high levels of ROS induced by DPA and DPA combined with HW treatment in Valencia orange fruit.

Browning, which is a result of oleocellosis, seems mainly the result of oxidation and polymerization of free phenolics, starting with the activity of PPO. Hui Wei et al.[30] found that DPA could effectively decrease the superficial scald of ‘Dangshansuli’ pear by inhibiting PPO activity and phenols content. Total phenols content and PPO activity were inhibited by DPA treatment at the later storage. Similar phenomena were also observed in relevant studies on other fruits[24,28-29,33].

Collapse and discolouration score was significantly reduced by DPA and DPA combined with HW treatment in Valencia orange fruit, which might be due to the result of the lower MDA level, higher antioxidant enzyme activities related to plant defenses induced by DPA treatment. Meanwhile, PPO activity in DPA and DPA combined with HW treated fruit were inhibited in the later period of storage to prevent browning. Therefore, treatment with DPA shows great potential for controlling postharvest oleocellosis of Valencia orange fruit in commercial production.

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收稿日期:2013-06-15

基金项目:国家自然科学基金面上项目(31071618);重庆市科技攻关(应用技术研发类/重点)项目(cstc2012gg-yyjsB80003);

农业部公益性行业(农业)科研专项(201203034)

作者简介:刘丽丹(1986—),女,硕士,研究方向为农产品加工与贮藏工程。E-mail:liulidan86@126.com

*通信作者:曾凯芳(1972—),女,教授,博士,研究方向为农产品加工与贮藏工程。E-mail:zengkaifang@163.com