Journal of Applied Botany and Food Quality 87, 124 - 130 (2014), DOI:10.5073/JABFQ.2014.087.019 1 School of Agricultural and Food Engineering, Shandong University of Technology, Zibo, China 2 Environment and Plant Protection Institute, Chinese Academy of Tropical Agricultural Sciences, Danzhou, China Responses of postharvest broccoli (Brassica oleracea L. var. italica) florets to controlled atmospheres with varying CO2/O2 levels at different temperature Ling Li1, Zhengke Zhang2, Yanyin Guo1*, Binbin Nian1 (Received March 7, 2014) * Corresponding author Summary Controlled atmospheres (CA) have been widely used in postharvest storage of fruits and vegetables. The gas compositions of common CA are consisted of O2, CO2 and N2, postharvest storage condition with gas combination of O2 and CO2 was rarely studied. In this re- search, the effects of CA with different CO2/O2 levels, i.e. 70% O2 + 30 % CO2, 60 % O2 + 40 % CO2, 50 % O2 + 50 % CO2, 40 % O2 + 60 % CO2, 30 % O2 + 70 % CO2, and air (control) on the storage life and properties of broccoli during storage were investigated at dif- ferent temperatures including 0, 10 and 20 °C. Results showed that the storage period of air treatments at 0, 10 and 20 °C was 21, 12, and 4d. Treatments with 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C maximum inhibited respiration rate and ethylene production, maintain chlorophyll and ascorbic acid content, reduced the accumulation of acetaldehyde and ethanol, and extended the storage life of broccoli florets to 49, 31, and 14d compared to 21 d at 0 °C, 12 d at 10 °C and 4 d at 20 °C in air-treated broccoli. These results indicated that an appropriate CA with O2/CO2 might be a potential strategy for postharvest storage of broccoli heads, and the appropriate proportion of O2 and CO2 might vary with different temperature. Introduction Broccoli (Brassica oleracea L. var. italica) is a vegetable increas- ingly recognized as a nutritional source for vitamins, antioxidants, and anticarcinogenic compounds in the daily diet (Podsedek, 2007). However, broccoli is a highly perishable product, its sensory quality after harvest encounters a rapid yellowing and undesirable off-flavor under inappropriate storage conditions (deschene et al., 1991). In recent years, various methods have been tested to extend the shelf life and improve postharvest quality of broccoli, such as refrigera- tion (Toivonen, 1997), heat treatment (TeTsuya et al., 2005), etha- nol vapor (han, 2006), 1-methycyclopropene (1-MCP) application (yuan et al., 2010), modified atmosphere packaging (serrano et al., 2006), and controlled atmospheres (CA) (Fernández-León et al., 2013). Moreover, controlled atmosphere (CA) storage is also considered an effective technique for maintaining postharvest quality of broccoli (ThomPson, 2010), which inhibited respiration rate and ethylene production, delayed tissue turgidity, chlorophyll loss and undesirable compositional changes, reduced the incidence and severity of decay, and alleviated some physiological disorders (ThomPson et al., 2010; eason et al., 2007; Toivonen et al., 2004; Fernández-León et al., 2013). Numbers of studies noted that appropriate proportions of O2 and CO2 in CA condition of broccoli varied temperature, which demonstrated indicating that CA of broccoli is temperature-dependent (Toivonen et al., 2004; canTweLL et al., 1999; Jones et al., 2006). For ex- ample, for fresh broccoli packaging storage, the recommended con- dition was 18.8 % O2 + 2.5 % CO2 and 9.5 % O2 + 4 % CO2 at 4 and 10 °C, respectively (anneLie et al., 2004). In broccoli CA storage, the optimized gas concentration was 10 % O2 + 5 % CO2 at 1-2 °C (Fernández-León et al., 2013), and 2 % O2 + 6 % CO2 at 4 °C (Paradis et al., 1996). Our previous study showed storage with higher concentrations of O2 and CO2 (40 % O2 + 60 % CO2) atmo- spheres at 15 °C prolonged storage life of broccoli by approximately 4 fold (Guo et al., 2013). However, a combined effect of higher le- vels of O2/CO2 and temperatures on storage life of broccoli has not been tested yet. The objective of this study was to establish the suit- able CA conditions under different storage temperatures for extend- ing storage life and maintaining quality of broccoli. Materials and methods Raw material Two batches of broccoli florets (brassica oleracea L. var. italica) were harvested from field of Shouguang vegetable station, Shandong Province on 12 April 2012 and 15 April 2013, respectively. Healthy broccoli florets with diameter ranging from 13 to 15 cm were se- lected and stored in a walk-in cooler at 5 °C for pre-cooling for 4 h. Experimental treatments For each temperature treatment (0, 10 and 20 °C), pre-cooled broc- coli florets were divided into 6 groups with 30 broccoli heads per group, and each group divided into 3 parts for replications with 10 broccoli heads per replication. Each group broccoli florets of 3 replicates were placed into three 0.5 m3 sealable plastic containers, respectively, and each group of broccoli heads was connected to a constant flow (0.05 m3 min-1) of air (control), 70 % O2 + 30 % CO2, 60 % O2 + 40 % CO2, 50 % O2 + 50 % CO2, 40 % O2 + 60 %CO2, and 30 % O2 + 70 % CO2. The samples were stored at RH 80-90 % and 0, 10 and 20 °C, respectively, until the end of their storage peri- ods. During storage, gas composition was regularly checked using an FBI-Dansensor CheckPoint O2/CO2 (MR-07825-00, FBI-Dansensor America Inc.). The broccoli heads in each treatment during storage were randomly selected for evaluation of storage period and physio- logical attributes as described below. Storage period The end of storage period of broccoli heads was designated as the time when approximately 30 % yellow coloration appeared on the surface of the product (yuan et al., 2010; Xu et al., 2006) or off- flavor occurred (JorGe et al., 1995; dank et al., 1999). Determination of respiration rate and ethylene production Three broccoli heads from each treatment, were firstly kept at their storage temperature for 8 h after removal from CA conditions in order to eliminate interference of treatments on internal gases com- position, and then individually sealed in a 3.86-L plastic container equipped with septa for 1 h at 0, 10, or 20 °C, according to their storage temperature. Five milliliters of headspace gas was with- drawn from each container, and CO2 and C2H4 levels were detected O2/CO2 controlled atmospheres in broccoli 125 using a gas chromatograph (Varian CP-3800, Agilent Technologies, Lexington, MA, USA) equipped with a thermal conductivity de- tector (TCD, CO2) and a hydrogen flame ionization detector (FID, ethylene). The temperature of column oven, TCD, FID and injector were set to 50, 130, 150 and 180 °C, respectively. Respiration rate and ethylene production were expressed as mg kg-1 h-1 and μL kg-1 h-1, respectively. Determination of acetaldehyde and ethanol contents Acetaldehyde and ethanol levels were measured with static head- space gas chromatography (Varian CP-3800, Agilent Technologies, Lexington, MA, USA) following the method of Ji et al. (2010) and the FID was set at 250 °C. Acetaldehyde and ethanol contents were both expressed as mg kg-1. Determination of chlorophyll content and yellowing rate Chlorophyll content was measured according to moran (1982) with slight modifications. Briefly, 0.1 g of broccoli florets were ground with 10 mL ethanol (95 %), and then extracted in the darkness for 24~36 h until broccoli tissue became white. The supernatant was measured at 652 nm with UV-1750 spectrophotometer (Shimadzu). The total chlorophyll content was expressed as mg kg-1 FW. Yellowing rate was measured according the surface yellow area of treated broccoli heads. Ten broccoli heads from each treatment were pictured using canon camera (Canon PC1468, Canon Inc., Japan), and the average yellowing rate of each treatment was calculated us- ing Photoshop software (Adobe Photoshop CS5 software package). Determination of ascorbic acid (AA) contents Ascorbic acid (AA) content was analyzed with dinitrophenylhydra- zine (DNPH) method (Terada et al., 1978). Briefly, 0.5 g broccoli florets of each treatment was homogenated with 20 mL mixture acid (6 % metaphosphoric acid cantaining 2 mol L-1 acetic acid) and then centrifuged at 15,000 × g for 20 min. Thereafter, the supernatant was filtrated through filter paper. One mL of filtrated supernatant was mixed with 0.05mL of 0.2 % 2, 6-dichlorophenolindophenol and then maintained at room temperature for 1 h. One mL of 2 % thiourea and 0.5 mL of 2 % DNPH were added to the mixture and then heated at 60 °C for 3 h. 2.5 mL of 95 % H2SO4 was added to the mixture and cooled on the ice prior to reading the absorbance at 540 nm. Ascorbic acid content was expressed as g kg-1 FW. Statistical analyses These experiments were conducted on a completely randomized de- sign, and each treatment comprised three replicates. Data were ana- lyzed using SPSS 13.0 statistical software and significant differences among treatments were determined by least significant differences (LSD) test at P ≤ 0.05. Results Storage period Combinations of O2/CO2 prolonged the storage period of broccoli florets heads under different temperature (Tab. 1). Treatments of 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C showed maximum efficacy, by which the storage periods of broccoli heads were extended to 49, 31, and 14 d, respectively, compared to the storage period of air treatments at 0 °C for 21 d, 10 °C for 12 d and 20 °C for 4 d. In common conditions, broccoli heads treated with higher O2 such as 70 % O2 + 30 % CO2 behaved as yellow surface, while treated with higher CO2 such as 30 % O2 + 70 % CO2 behaved as off-flavors. Respiration rate and ethylene production Respiration rate in air and 70 % O2 + 30 % CO2-treated broccoli heads rapidly increased with the peaks under 0, 10, and 20 °C ap- peared at 14, 8, and 2 d, respectively (Fig. 1). Among treatments, 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C, strongly suppressed respiration rate, which was maintained at a relatively lower level compared to that in other treated broccoli. Ethylene productions of all treatments were in parallel with the changes of respiration rate (Fig. 2). Broccoli treated with 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C, showed a lowest and steady level of ethylene production. Acetaldehyde and ethanol contents Overall, acetaldehyde and ethanol contents in all broccoli florets showed a gradual increase trend with extension of storage time (Fig. 3, Fig. 4). Differently, among all treatments, acetaldehyde and ethanol contents in broccoli florets treated with 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C, showed a the lowest level during whole storage (Fig. 3, Fig. 4). Chlorophyll content and yellowing rate Chlorophyll contents of all treated broccoli florets declined during storage time, and lower temperature optimum delayed the chloro- phyll loss (Fig. 5). For example, during 0-14 d of storage time, the chlorophyll content of broccoli florets treated with 40 % O2 + 60 % CO2 declined by 6.0 % compared to 13.8 % and 16.4 % at 0,10 and 20 °C, respectively. In general, the chlorophyll content of broccoli florets treated with 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C, showed the lowest decline trend, compared with the other treatments at their respective storage temperature. Yellowing rate of broccoli florets of all treat- ments showed a reverse trend of that of chlorophyll content (Fig. 5 and 6). Ascorbic acid (AA) contents Changes of AA content of broccoli florets were familiar with chlo- rophyll content (Fig. 5 and 7). Among the treatments of their tem- perature, the least loss of AA content of broccoli florets was 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C. Furthermore, lower temperature could signifi- cantly delay the loss of AA content. During 0-14 d of storage time, the AA content of broccoli florets treated with 40 % O2 + 60 % CO2 at 0, 10, and 20 °C, was declined by 5.7 %, 13.6 %, and 19.0 %, respectively. Tab. 1: Storage period of broccoli florets treated with varied O2/CO2 concen- tration under different temperature. Different little letters indicates that there is significant difference among treatments. Storage period (d) Treatments Storage temperature (°C) 0 10 20 70 % O2 + 30 % CO2 35c 8f 3e 60 % O2 + 40 % CO2 49a 28b 8c 50 % O2 + 50 % CO2 42b 31a 10b 40 % O2 + 60 % CO2 35c 24c 14a 30 % O2 + 70 % CO2 21e 20d 8c Air 28d 12e 4d 126 L. Li, Z. Zhang, Y. Guo, B. Nian Fig.1 Fig.2 Fig. 1: Respiration rate of broccoli heads treated with varying O2/CO2 levels at different temperature. Vertical bars indicate the standard deviations for each treatment (n=5). Air treatment was used as control. Fig. 2: Ethylene production of broccoli heads treated with varying O2/CO2 levels at different temperature. Vertical bars indicate the standard de- at different temperature. Vertical bars indicate the standard de-at different temperature. Vertical bars indicate the standard de- different temperature. Vertical bars indicate the standard de- viations for each treatment (n=5). Air treatment was used as control. Discussion The optimal atmospheres proportion in CA storage of broccoli was different when storage temperature was diverse. It has been reported that the proper gas concentration was 10 % O2 + 5 % CO2 at 1-2 °C (Fernández-León et al., 2013), while combination of 2 % O2 and 6 % CO2 was the most appropriate for broccoli preservation when stored at 4 °C (Paradis et al., 1996). High O2 (30 %-80 %) has a favorable effect on preservation of fruits and vegetables, which could extend shelf life of ‘Yaoshan’ pears (Li et al., 2012), and high CO2 could inhibit the accumulation of off-flavor substances during iceberg lettuce storage (heimdaL et al., 1995). However, adverse effects also were found in other postharvest crops. For instance, 60-100 % O2 treatment accelerated the decay of Chinese bay-berry, strawberry and blue berry (zhenG et al., 2008), and increased the loss of green color and chlorophyll pigments (LaXman et al., 2012). For high CO2 treatments, studies of Yasutaka (yasuTaka et al., 1990) showed that treatment with 20 % O2 + 60 % CO2 + 20 % O2/CO2 controlled atmospheres in broccoli 127 Fig.3 Fig.4 N2 for 24 h significantly reduced respiration rate and ethylene pro- duction, and delayed off-flavor and decay in broccoli, tomato, and peach. However, kader (1995) pointed out that inappropriate high CO2 might result in CO2 injury or physiological disorder such as off- flavor, which involved in the accumulation of acetaldehyde, ethanol and a tiny part of other volatiles (James et al., 2000; ke et al., 1990). Present study exhibited that high proportion of O2/CO2 such as 70 % O2 + 30 % CO2 accelerated chlorophyll loss and yellowing. On the other side, extreme high CO2 in CA condition such as 30 % O2 + 70 % CO2 rapidly accumulated acetaldehyde and ethanol, indicat- ing that inappropriate high CO2 could result in off-flavor of broccoli florets. Only appropriate combinations of O2 and CO2 including 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C, provided the most effective ways to maintain quality and reduce off-flavor, as indicated by reductions in chlorophyll loss and the acetaldehyde and ethanol. Results implied that the similar proportioning with high levels of O2 and CO2 in CA storage under a wide range of temperature (0-20 °C) might be an ap- propriate strategy for broccoli storage. In conclusion, the optimum proportion of O2 and CO2 to the storage Fig. 3: Acetaldehyde contents of broccoli heads treated with varying O2/CO2 levels at different temperature. Vertical bars indicate the standard de- at different temperature. Vertical bars indicate the standard de-at different temperature. Vertical bars indicate the standard de- different temperature. Vertical bars indicate the standard de- viations for each treatment (n=5). Air treatment was used as control. Fig. 4: Ethanol contents of broccoli heads treated with varying O2/CO2 levels at different temperature. Vertical bars indicate the standard deviations for each treatment (n=5). Air treatment was used as control. 128 L. Li, Z. Zhang, Y. Guo, B. Nian Fig.5 Fig.6 and of broccoli varied with temperature. The best treatments of O2/ CO2 were found to be 60 % O2 + 40 % CO2 at 0 °C, 50 % O2 + 50 % CO2 at 10 °C, and 40 % O2 + 60 % CO2 at 20 °C. These treatments could inhibit respiration rate and ethylene production, maintain chlo- rophyll and ascorbic acid content reduce the accumulation of acet- aldehyde and ethanol, and extended the shelf life of broccoli to 49, 31, and 14, respectively. Furthermore, temperature played a critical factor on the preservation period of broccoli florets, with treatment of 60 % O2 + 40 % CO2 at 0 °C showed the best efficacy in extending storage life among all treatments at 10 and 20 °C. 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