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Physicochemical and biochemical characterization of ripening in jujube (Ziziphus mauritiana Lamk) fruits from two accessions grown in Guadeloupe
Scientia Horticulturae 175 (2014) 290–297
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Physicochemical and biochemical characterization of ripening in jujube (Ziziphus mauritiana Lamk) fruits from two accessions grown in Guadeloupe S. Zozio a,b , A. Servent b , O. Hubert a,b , A. Hiol c , D. Pallet b , D. Mbéguié-A-Mbéguié a,b,∗ a
CIRAD, UMR QUALISUD, F-97130 Capesterre-Belle-Eau, Guadeloupe, France CIRAD, UMR QUALISUD, F-34398 Montpellier, France c CIRAD, UMR QUALISUD Université de la Réunion – ESIROI, Spécialité agroalimentaire, PTU 97490 St Clotilde, France b
a r t i c l e
i n f o
Article history: Received 18 March 2014 Received in revised form 11 June 2014 Accepted 12 June 2014 Available online 11 July 2014 Keywords: Ethylene production Fruit ripening Jujube Ziziphus mauritiana
a b s t r a c t Jujube fruits (Ziziphus mauritiana Lamk) from two accessions grown in Guadeloupe were harvested and sampled at five ripening stages, from green to reddish-brown in colour. Their physiological characteristics were then investigated. Ascorbic acid increased with ripening until stage 4, to 463 mg/100 g and 168 mg/100 g dry weight, for cultivars P3 and P5, respectively. Likewise, ethylene production increased until stage 4, to 121 l/kg/h and 116 l/kg/h, for cultivars P3 and P5, respectively. High and transient sucrose accumulation was observed during ripening of P3 fruits, concomitantly with low and constant glucose and fructose contents. P5 fruits also accumulated sucrose transiently but at a lower level than P3 fruits, with a marked decrease at the end of ripening. In contrast to P3 fruit, glucose and fructose accumulated continuously to high levels during P5 fruit ripening. These data suggested differential sucrose metabolism during ripening of these fruits. Postharvest treatments with 1-MCP and acetylene were also performed on the three first ripening stages of both cultivars P3 and P5. On the basis of the findings, we discuss the climacteric behaviour of the P3 and P5 ripening process. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Jujube (Ziziphus mauritiana Lamk), commonly known as “pomme-surette” in Guadeloupe, is widely distributed in the southern and northern parts of the island. The jujube tree, which belongs to the Ziziphus genus and the Rhamanceae family, is widespread throughout tropical and subtropical regions of Asia, Africa and Australia. Two major Ziziphus species are domesticated: Ziziphus mauritiana Lamk., the Indian jujube which is commonly known as Ber, and Ziziphus jujuba Miller, the Chinese jujube (Azam-Ali et al., 2006). Depending on the ripening stage, the jujube fruit peel colour shifts from green to yellow, and then from a reddish to brown colour. Generally, the fruit is eaten fresh and has a mild bittersweet flavour. Jujube is considered a functional fruit due to its high
∗ Corresponding author at: CIRAD, UMR QUALISUD, F-97130 Capesterre-BelleEau, Guadeloupe, France. Tel.: +590 590 86 17 70; fax: +590 590 86 80 77. E-mail addresses: [email protected] (S. Zozio), [email protected] (A. Servent), [email protected] (O. Hubert), [email protected] (A. Hiol), [email protected] (D. Pallet), [email protected], [email protected] (D. Mbéguié-A-Mbéguié). http://dx.doi.org/10.1016/j.scienta.2014.06.014 0304-4238/© 2014 Elsevier B.V. All rights reserved.
nutritional value. However, the shelf-life of jujube fruits is short (2–4 days at ambient temperature) and its rapid perishability was reported to be problematic for fruit postharvest management and advance processing (Pareek et al., 2009). The fruit quality traits depend on how the physiological development and ripening process occurs in the field and after harvesting. Consequently, characterizing this process and gaining further insight into the related physiological basis are essential prerequisites with a view to postharvest management and improving the fruit quality. Nevertheless, and in contrast to the Chinese jujube (Ziziphus jujuba Miller), only a few studies have been devoted to the Ziziphus mauritiana Lamk ripening process. The putative variability of the ripening process within the Ziziphus species has thus yet to be determined. With regard to their ripening behaviour, the few studies performed within the Ziziphus species, based on the ethylene production and respiration rate, suggested that Z. mauritiana and Z. spina-christi (L.), i.e. a wild native Iraqi species, exhibited climacteric ripening (Abbas and Fandi, 2002; Sharma et al., 2000), whereas Z. jujuba was recognized as being non-climacteric (Sheng et al., 2003; Zhang et al., 2009). The number of edible fruits in Guadeloupe has been estimated as up to 130, with high variability (Lebellec and Lebellec, 2007).
S. Zozio et al. / Scientia Horticulturae 175 (2014) 290–297
However, heritage fruit of Guadeloupe has not been markedly promoted, apart from banana which is mainly grown for export. In order to promote this heritage fruit, we attempted to gain further insight into the quality properties of jujube (Ziziphus spp.), in order to investigate the potential value of this fruit as a fresh and/or processed product. Several of jujube fruit plots were identified in Guadeloupe, indicating that these fruits were exploited in the past by the island’s inhabitants. In this study, we physico-chemically characterized the ripening process of jujube fruit from two different accessions growing side by side in Guadeloupe. In addition to the ethylene and respiration criteria considered in previous studies, we combined postharvest 1-MCP, a well known ethylene binding inhibitor (Sisler and Serek, 1997), and acetylene, together with biochemical changes, to assess the ripening behaviour of the respective ripening process. The data obtained were further discussed in regard to the contrasted morphological features, including colour, firmness or size and nutritional attributes of these fruits, as highlighted previously (Zozio et al., 2013). 2. Materials and methods 2.1. Plant material 2.1.1. Fruit harvest for in planta analysis Two jujube fruit trees (Ziziphus mauritiana Lamk), identified as P3 and P5, that were at least 30 years old according to the farmers, were chosen based on the basis of their morphological features and global fruit taste. The P3 tree yielded sweet oblong fruit, while the P5 tree had bitter round fruit (Fig. 1). Fruits were harvested from each tree between January and February, corresponding to their optimal fructification period. Because of their desynchronized flowering and fruit development and ripening in planta, fruits of each tree were harvested manually by shaking the tree, on the same day, and sampled into five development stages according to their colour and size (Fig. 1). Some of the fruits were used to measure ethylene production, colour, size and firmness. Others were freezedried and kept under vacuum until use for biochemical analyses. 2.1.2. Fruit harvest for the postharvest investigation Based on the sampling described above, the first three ripening stages were chosen to study off-tree ripening in air at 20 ◦ C, and after postharvest treatment with 1-MCP and acetylene. 2.1.3. Post-harvest treatment Fruits sampled at the three first developmental stages were treated separately with 1000 ppm of acetylene and 0.5 ppm of 1MCP. The treatment was performed for 24 h at 20 ◦ C using a 35-l Plexiglas container. 1-MCP was prepared from a commercial powder provided by RHOM HASS (Pont Du Casse, France) according to the manufacturer’s instructions. Untreated fruits used as control were stored simultaneously in air under the same conditions. After acetylene- and 1-MCP treatments, fruits were kept to in a ripening chamber at 20 ◦ C. A sample of each treated fruit, and controls, were picked daily until the fruits reached the end of maturation (=0 l/kg/h of ethylene production) which was 6 and 7 days for P3 and P5, respectively. At this stage, the fruit samples were then freeze-dried for the sugar and organic acid analyses. 2.2. Physicochemical analysis 2.2.1. Ethylene measurement Ethylene production was measured during in planta and ex planta ripening according to the method described by (Chambroy et al., 1995). Approximately 30 fruits from each ripening stage were sealed in a 1–2 l glass container for 1 h at 20 ◦ C. A 100 l gas sample was withdrawn from the headspace using a gas-tight
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hypodermic syringe (Interchim, Montluc¸on, France) and analyzed using a CP-3800 gas chromatograph (Varian, Courtaboeuf, France) equipped with a flame ionization detector. Gas analysis was performed on a capillary PLOT fused silica column 25 m × 0.53 mm (Varian, Courtabeauf, France) under the following conditions: oven temperature 40 ◦ C, FID dectector temperature 150 ◦ C, helium as gas carrier (30 ml/min) and make up (20 ml/min), hydrogen at 4.5 bar and air at 300 ml/min. Ethylene concentrations were calculated from the calibration ethylene standard curve, and the results are expressed as l/kg/h. Experiments were performed on three biological replicates.
2.2.2. Firmness, colour and fruit size: in planta measurements Fruit firmness was measured in the equatorial region using a TAXT2 penetrometer (Swantec, Gennevilliers, France) and peel colour was measured as described by Bruno-Bonnet et al. (2013). The hue angle value (h◦ ) was used to assess the colour change with bluishgreen at 180◦ , yellow at 90◦ , and red-purple at an angle of 0◦ . The peel colour was measured at the apex of 15 fruits. Fruit size was measured on about 30 fruits from each ripening stage, as described by Dadzie and Orchard (1997), using a Vernier calliper (Mitutoyo, Roissy, France).
2.3. Biochemical analysis of in planta and ex planta fruit ripening after postharvest treatment 2.3.1. Organic acid determination Organic acids were extracted with H2 SO4 2.5 mM using a ratio of 0.5 g of dry matter to 10 mL of sulfuric acid. The mixture was agitated for 20 min with a Reax 2 shaker (Heidolph, Schwabach, Germany), then centrifuged for 10 min at 3300 × g (10 ◦ C) using a 5810R Eppendorf centrifuge (Le Pecq, France). HPLC analysis was performed on Agilent System 1200 series HPLC (Agilent 1200 HPLC system, Massy, France) using an HyperREZTM XP Carbohydrate Column H+ Ion Counter, 8 m, 8% cross linkage, 7.7 × 300 mm (ThermoScientific, Rochester, USA) with 0.05 M H2 SO4 as mobile phase at a 0.8 ml/min flow rate. The acids were identified by comparison of their retention times with standard (Supelco, Bellefonte, USA).
2.3.2. Sugar determination Soluble sugars were separated by high performance ionic chromatography (HPIC) as described by Gibert et al. (2013).
2.3.3. Ascorbic acid (AA) content Ascorbic acid content was assessed using the method of Mertz et al. (2010) with some modifications. Ascorbic acid was analyzed using an Agilent System 1200 series HPLC (Massy, France) with a ZORBAX Eclipse Plus C18 column (5 m, 4.5 × 250 mm, Agilent, Massy, France). The operating conditions were as follows: isocratic solvent system using a 0.01% solution of H2 SO4 at a 1 mL/min flow rate, 20 L injection volume, and detection was set at 245 nm. Extractions and analysis were carried out in triplicate. Ascorbic acid was quantified by external standard calibration. The results are expressed in mg AAS /100 g.
2.4. Statistical analysis The data were subjected to analysis of variance (ANOVA) using Statistica software (Statsoft, version 7). The means were separated by Duncan’s multiple range test (p < 0.05). Analyses were performed on three biological replicates.
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Fig. 1. Morphological features of jujube fruits from P3 and P5 accessions grown in Guadeloupe. Jujube fruits were harvested from plants grown on a local farm based in the southern part of the island and under natural conditions. Then they were grouped according to their colour and form.
3. Results 3.1. Physicochemical and biochemical changes during in planta ripening Physicochemical changes during jujube fruit were assessed through ethylene production, colour firmness and fruit diameter measurement (Table 1). The level of ethylene production increased transiently, with a peak at 121.46 ± 1.55 l/kg/h for cultivar P3, and 116.75 ± 2.18 l/L/kg/h for cultivar P5. Interestingly, both reached the peak at stage 4, and then the production decreased sharply. At the first harvest stage, the hue value was 114◦ ± 1.55 and 112◦ ± 2.67 for cultivars P3 and P5, respectively. A significant decrease in hue value was observed between ripening stages 3 and 4 for cultivar P3 (20%), and between stages 2 and 3 for cultivar P5 (33%) (p < 0.05). At the late ripening stage, fruits of both cultivars exhibited a comparable hue value (65◦ and 67◦ ) (Table 1). Concerning the fruit firmness, cultivars P3 and P5 exhibited a differential softening pattern during ripening. Cultivar P3 remained firmer during ripening, while the firmness in P5 fruits began to decrease drastically by 67% (11.89 N ± 1.39–4.37 N ± 0.71 p < 0.05) at stage 3 (Table 1). For both cultivars P3 and P5, fruit size increased slightly at a comparable level during in planta ripening. At the late ripening stage, the size of both cultivar P3 and P5 fruits exhibited a comparable diameter of approximately 29 mm, which is in accordance with previously reported data (Gupta et al., 2004; Meena et al., 2009) (Table 1). Sugar content changes are described in Table 2. During in planta ripening of P3 fruit, sucrose accumulated to a maximum level reached at stage 4, before decreasing slightly to 30% at stage 5, as also reported by Abbas and Fandi (2002). The sucrose level was 5- and 7-fold higher than the glucose and fructose levels, respectively. However, no marked changes were observed in glucose and fructose levels throughout ripening. For P5 fruit, the sucrose accumulation pattern was similar but at a lower level, with a drastic decrease (92%) at ripening stage 5. At this stage, P5 fruit accumulated 3-fold more glucose and fructose than P3. The ascorbic acid analysis revealed a significant and higher ascorbic acid content in cultivar P3 than in P5. Similar to the ethylene pattern, an increase in ascorbic acid was observed until the 4th stage for cultivars P3 and P5 (463.61 ± 13.93 and 258.78 ± 4.37 mg/100 g, respectively), and then a decrease was observed. The decrease in the hue angle observed in cultivar P3 and P5 was correlated with the ripening pattern (Table 2).
Malic acid was the most abundant of all the organic acids analyzed in both cultivars P3 and P5, while tartaric acid was the least abundant. Concerning the two major acid components, i.e. malic and citric acid, both accessions accumulated a comparable level of citric acid, whereas cultivar P5 exhibited a higher level of malic acid than cultivar P3 (25% for stage 1 and 60% for stage 5). For cultivars P3 and P5, the citric acid level decreased slightly from stage 1 to 5, while the tartaric acid level increased. Transient accumulation of malic acid was observed during the ripening of both P3 and P5 fruits, with a maximum observed at stage 2. 3.2. Effects of postharvest treatments on fruit ripening and related biochemical changes Postharvest ripening of P3 and P5 fruits was investigated in fruit sampled at the first three development stages. Fruits from each cultivar were treated with 1-MCP or acetylene, and left to ripen in air at 20 ◦ C until decay, which occurred at 6 days for cultivar P3 fruits and at 7 days for cultivar P5. Untreated fruits sampled at the same developmental stage were used as control. For each cultivar, postharvest ripening was monitored daily by measuring ethylene production at the same time. According to the developmental stages, postharvest treatments differentially affected the ethylene production of cultivar P3 and P5 fruits (Fig. 2). For fruit harvested at the 1st ripening stage, only acetylenetreated cultivar P5 fruits produced a higher level of ethylene than 1-MCP-treated and control fruits, from which the ethylene levels were comparable. However, no marked change was observed in cultivar P3 fruits, irrespective of the postharvest treatment (Fig. 2A and D). At the 2nd stage for cultivar P3, the ethylene level increased, regardless of the treatment, 24 h after treatment (Fig. 2B). A transient ethylene production peak was observed at 72 h for acetylene-treated and control fruits, while for 1-MCP-treated fruits, the peak was reached later at 96 h. Maximum ethylene production was higher in acetylene-treated fruits compared to control and 1-MCP-treated fruits. For cultivar P5, the ethylene production pattern was similar to that observed for fruits sampled at stage 1 (Fig. 2E). Ethylene production increased continuously regardless of the treatment. However, the ethylene level was higher with acetylene-treated fruits than for the 1-MCP-treated and control fruits. For fruits harvested at an advanced ripening stage (stage 3), cultivars P3 and P5 exhibited different ethylene production patterns.
S. Zozio et al. / Scientia Horticulturae 175 (2014) 290–297
A
D 0 a 1-MCP a Acethylene a
24 a a a
Control
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140 Ethylene producon (μl/Kg/h)
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Fig. 2. Effects of postharvest treatment (1-MCP and acetylene) on ethylene production rates of P3 (A–C) and P5 (D–F) tree fruits harvested at stages 1 (A and D), 2 (B and E) and 3 (C and F). Fruits were exposed to 0 (control) or 0.5 ppm 1-MCP or 1000 ppm acetylene for 24 h, and then kept in air at 20 ◦ C and 80–90%. Each point represents the mean of three replicates ± SE. HT: harvest time. The table above each graph shows the significant difference during ripening for one treatment.
For cultivar P3, a similar ethylene production pattern was observed regardless of the treatment, with a transient ethylene production peak reached at 24 h for the control and acetylene-treated fruits, and at 48 h for 1-MCP treated fruits. For cultivar P5, the control and treated fruits exhibited a similar ethylene production pattern, with a transient peak at 48 h after treatment (Fig. 2F).
Remarkably, acetylene-treated P5 fruits reached an ethylene level at 72 h (119.7 ± 11.5 l/kg/h) similar to that of the stage 4 fruits harvested on the tree (116.7 ± 2.1 l/kg/h). However, the control reached only 94.3 ± 3.8 l/kg/h (Fig. 2F). Furthermore, this increase was not observed in treated P3 fruits.
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Table 1 Ethylene production, ascorbic acid and some physical characteristics assessed during in planta ripening (stages 1–5) of jujube fruits from trees P3 and P5. The value in brackets is the standard deviation. Characteristics
Ripening stages in planta Cultivar P3
Ethylene production (l/kg/h) Skin hue angle (◦ ) Firmness (N) Fruit diameter (cm)
Cultivar P5
1
2
3
4
5
1
2
3
4
5
1.84 (0.26) 114.15 (1.55) 10.97 (1.80) 23.48 (1.61)
5.59 (0.14) 110.42 (2.53) 9.97 (1.32) 27.48 (2.20)
40.04 (5.48) 104.29 (3.73) 9.47 (1.63) 27.52 (1.56)
121.46 (1.55) 82.55 (4.62) 9.13 (1.52) 30.61 (2.13)
0.00 (0.00) 65.39 (2.35) 7.55 (1.21) 30.86 (2.06)
0.00 (0.00) 112.53 (2.67) 12.69 (1.06) 23.44 (1.00)
1.12 (0.07) 108.05 (2.20) 13.14 (1.51) 26.79 (1.71)
26.80 (1.23) 90.90 (2.04) 11.89 (1.39) 27.78 (1.96)
116.75 (2.18) 72.07 (4.96) 4.37 (0.71) 27.81 (2.72)
0.00 (0.00) 66.68 (3.81) 3.16 (0.58) 28.41 (2.09)
Table 2 Ascorbic acid (mg/100 g), organic acid (mg/g) and sugar (mg/g) contents after the maturation of P3 and P5 fruits sampled at the three first ripening stages and treated with 1-MCP and acetylene, and left in a maturation chamber at 20 ◦ C until the last ripening stage (5). Ripening stages in planta Cultivar P3
Ascorbic acid (mg/100 g) Organic acids (mg/g) Citric acid Tartaric acid Malic acid Sugars (mg/g) Glucose Fructose Sucrose
Cultivar P5
1
2
3
4
5
1
2
3
4
5
200.61 (10.92)
322.48 (3.10)
387.40 (3.11)
463.61 (13.93)
158.50 (1.12)
114.69 (1.35)
137.11 (0.91)
168.59 (30.20)
258.78 (4.37)
184.85 (0.10)
49.46 (2.14) 5.08 (0.59) 81.36 (3.42)
33.18 (5.44) 6.88 (1.87) 66.04 (3.09)
27.60 (4.25) 9.17 (1.48) 47.51 (4.94)
46.65 (5.00) 6.88 (1.50) 97.18 (7.00)
44.46 (7.00) 5.91 (1.22) 103.14 (7.00)
29.93 (3.00) 6.48 (1.60) 101.86 (7.50)
25.89 (6.68) 7.39 (1.23) 87.29 (9.71)
24.76 (7.76) 9.16 (1.48) 76.20 (6.24)
90.36 (1.11) 92.18 (0.75) 266.26 (4.30)
71.83 (1.49) 82.88 (0.41) 109.84 (4.13)
150.78 (12.70) 158.85 (12.05) 248.71 (6.29)
107.39 (2.28) 110.43 (3.36) 248.51 (4.67)
123.72 (7.94) 126.44 (7.65) 238.90 (7.14)
267.53 (5.82) 261.96 (6.24) 17.70 (0.85)
46.71 (5.27) 3.26 (1.31) 77.91 (5.12) 82.85 (0.92) 90.51 (0.66) 259.06 (4.62)
82.65 (2.86) 89.12 (3.65) 359.41 (20.83)
The italics characters correspond to standard deviation values.
76.78 (0.27) 81.60 (1.15) 383.98 (9.65)
30.86 (6.78) 8.58 (1.06) 60.70 (8.04) 78.94 (2.24) 80.44 (2.21) 386.69 (25.47)
S. Zozio et al. / Scientia Horticulturae 175 (2014) 290–297
The italics characters correspond to standard deviation values.
S. Zozio et al. / Scientia Horticulturae 175 (2014) 290–297
Tartaric Acid b
b a
a
a
a a
a
a
a
a
a
a a
a
a
b a
a a
b
b
b
a a
a
a
Sugar mg/g of DM
A
a
250
A
200
aa
a
sucrose
a aa
a bb
150
c
ba
c
b
a
a
b
100 50
a
b
b
0
2
3
1
Control
2
3
1
1-MCP Treatments
Citric acid Organic acids mg/g of DM
fructose
300
1
140 120 100 80 60 40 20 0
glucose
Malic Acid
Tartaric acid
2
3
1
a
300
b
a a
a
b b
a
a
a
a
b
b b
a
a
1
2
3
1
1-MCP
2
3
Acetylene
Treatments
Malic acid
a
3
Control
B a
2
Acetylene
a
a
a
a
a
a
a
a
a
1
2
3
1
2
3
1
2
3
Sugar mg/g of DM
Organic acid mg/g of DM
Citric Acid 140 120 100 80 60 40 20 0
295
250
glucose
B
200
fructose aa
aa a
150
a bb
aa
1
2
a b
b
aa
bb
a 100 50 0
Control
1-MCP
1
3
Control
Acetylene
3
1-MCP
1
2
3
Acetylene
Treatments
Treatments Fig. 3. Organic acid content in jujube fruits from cultivars P3 (A) and P5 (B) measured at the end of ex planta maturation at 20 ◦ C. Fruits were sampled at stages 1–3 for 24 h treatments with 1-MCP and acetylene, and then left in a maturation chamber for 6 days for P3 fruits and 7 days for P5 fruits. The control represents untreated fruits. The values are expressed in mg of acid per g of dry matter. Different letters (a, b, c) express the significant effect of treatment (1-MCP and acetylene vs. control) for one ripening stage using Duncan’s multiple range test at p < 0.05.
2
Fig. 4. Content of sugars identified in jujube fruits from cultivars P3 (A) and P5 (B) measured at the end of ex planta maturation at 20 ◦ C. Fruits were sampled at stages 1–3 for 24 h treatments with 1-MCP and acetylene, and then left in a maturation chamber for 6 days for P5 fruits and 7 days for P5 fruits. The control represents untreated fruits. The values are expressed in mg of sugar per g of dry matter. Different letters (a, b, c) express the significant effect of treatment (1-MCP and acetylene vs. control) for one ripening stage using Duncan’s multiple range test at p < 0.05.
4. Discussion The sugar as well as organic acid per dry matter levels was also measured in order to check the biochemical changes during ripening of P3 and P5 jujube fruit. Accumulation in control fruits showed that their level was differentially affected by the postharvest storage conditions described in this study, according to the fruit physiological stage at harvest and the accession (Figs. 3 and 4). For all P3 and P5 fruits tested, compared to their physiological stage at harvest, postharvest storage increased by up to 2-fold the tartaric acid level, and up to 2–3-fold the glucose and fructose level (2–3-fold each). For P3 fruits, the malic acid level decreased slightly (up to 1.4-fold) for P3 fruits at all physiological stages while, for P5 fruits, this decrease was observed only in fruits sampled at stage 3. For both P3 and P5 fruits, the postharvest storage conditions induced a drastic decrease in sucrose content (up to 36-fold for P3), while no trace was detected in P5 fruits. Citric acid accumulation varied according to the physiological stage at harvest. For fruit sampled at the first physiological stage, the postharvest storage conditions increased the citric acid level by 1.2-fold only at stage 1 for P3, and at stages 1 and 2 for P5 fruits, respectively. The effect of acetylene and 1-MCP on the biochemical content was also investigated in this study. As compared to the controls (untreated fruits), no marked changes were observed in all other biochemical contents in acetylene and 1-MCP treated fruits, except for citric acid in P5 fruits. Acetylene-treated fruits exhibited a higher citric acid level (1.5-fold on average) than 1-MCP treated fruits, whose citrate content was comparable to that of the controls.
In this study, we carried out physicochemical and biochemical characterizations of the ripening process in jujube fruits from two accession trees, with contrasting morphological features, grown in Guadeloupe. During in planta ripening, both P3 and P5 fruits exhibited a similar ethylene production pattern characterized by a transient ethylene peak at stage 4, in agreement with previously reported data (Abbas and Fandi, 2002; Al-Niami et al., 1992; Lal, 2005; Kaur et al., 2008; Qiuping and Wenshui, 2007; Sharma et al., 2000). However, contrasted patterns were noted in terms of softening, with P3 fruits being firmer during ripening than P5 fruits. Moreover, during their respective in planta ripening processes and compared to P5 fruit, P3 fruits accumulated on average 2-fold more ascorbic acid and sucrose. The ascorbic acid content and sucrose/(glucose + fructose) ratio, primarily due to the sucrose content, could thus be considered as a biochemical indicator of P3 and P5 fruit ripening. Taken together, our data indicated that the various morphological features of the P3 and P5 accessions were also reflected in the fruit ripening process and the corresponding biochemical changes. Considering that the P3 and P5 accessions had been planted more than 30 years earlier and had been growing in the same agroclimatic region, our data suggest that the P3 and P5 accessions were probably different Z. mauritiana cultivars. However, it would be interesting to confirm this hypothesis through genetic diversity analysis. With regard to the climacteric behaviour of the jujube fruit ripening process, previous studies reported contrasting data on the general trend, ascribing the climacteric nature to a concomitant respiration crisis with a burst of ethylene synthesis. Abbas and
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Fandi (2002) reported climacteric behaviour in the Z. mauritiana cultivar Zaytoni, while Sheng et al. (2003) and Zhang et al. (2009) reported non-climacteric behaviour in Zizyphus jujuba. However, the climacteric features of Zizyphus fruit cannot be clearly related to the species, as the Zizyphus jujuba Jing cultivar is reported to exhibit climacteric ripening 1 behaviour (Jiang et al., 2003). To assess the climacteric behaviour of P3 and P5 accession fruits, we examined the ethylene production of both P3 and P5 fruits sampled at different developmental stages and treated with acetylene (an ethylene analogue) and 1-MCP, an inhibitor of ethylene action (Sisler and Serek, 1997). Our data suggested that the ripening process of jujube fruit from P3 and P5 accessions undergoes climacteric behaviour in different ways. Ethylene production of cultivars P3 and P5 fruits was affected differentially by acetylene and 1-MCP, according to the developmental stage, thus supporting the hypothesis that the P3 and P5 accessions are probably different cultivars. For P3 accession fruits, 1-MCP treatment induced a delay in ethylene production during postharvest ripening at stages 2 and 3 as compared to acetylene-treated and control fruits. At stage 2, acetylene treatment increased fruit ethylene production, which reached an early peak (72 h after treatment), while that of 1-MCP treated fruits was obtained later (96 h after treatment). At stage 3, a transient ethylene peak was reached earlier in control and acetylene-treated fruits than in 1-MCP treated fruits. These data suggested that P3 fruits exhibited climacteric behaviour. Surprisingly, when harvested at an earlier developmental (stage 1), P3 fruits treated with acetylene and 1-MCP produced ethylene at comparable levels, higher than the control, with a similar pattern. We could not explain this atypical ethylene production pattern. The P5 accession of jujube fruit exhibited climacteric behaviour earlier, since the antagonistic effect of 1-MCP and acetylene was first observed at stage 1, and was exacerbated at stage 2. In contrast, at stage 3, the antagonistic effect of 1-MCP and acetylene on ethylene production was less marked between treatments than in fruit harvested at stages 1 and 2. The ethylene responsiveness of the fruit might have been complete enough to be affected by our 1-MCP treatments. Note also that under our postharvest conditions, and regardless of the developmental stage at harvest, the decrease in ethylene production used here as a physiological indicator of the late ripening stage occurred at 6 and 7 days for P3 and P5 fruits, respectively. Al-Niami et al. (1992) reported a similar storage life for two other jujube varieties. As compared to the control fruit, these data indicated that the level of ethylene fruit responsiveness at harvest impacts the level of fruit ethylene production during postharvest storage, as discussed previously, while not affecting the fruit storage life. Previous studies showed a drastic decline in respiration rate at the end of storage life, suggesting a putative relationship between respiration and storage life duration (Abbas, 1997; Al-Niami et al., 1992). We are, however, unable to discuss this hypothesis here due to the lack of jujube fruit respiration data in this study, as well as the insufficient data on the organic acid compound related to respiration (i.e. malate). Postharvest storage, acetylene and 1-MCP treatment also differentially affected other biochemical compounds in P3 and P5 fruits. Our postharvest storage conditions induced the accumulation of some biochemical compounds, including glucose, fructose and tartaric acid, while others such as sucrose were completely eliminated. Neither ethylene nor 1-MCP affected the sugar and tartaric acid content in P3 and P5 fruit, citric acid in P3 fruit or malic acid in P5 fruit, suggesting that the metabolism of these components are under ethylene independent regulation. We failed to explain the rise in malic acid content in acetylene- and 1-MCP-treated P3 fruits to a similar level as in the controls. In contrast, citric acid, whose content was induced in P5 acetylene-treated fruit as compared to control and 1-MCP-treated fruits, is probably positively regulated by ethylene in this accession.
5. Conclusion In this study, we characterized jujube fruit from two accession trees (P3 and P5) grown in Guadeloupe. Our data led us to conclude that these two accessions were probably two different cultivars. The study of the relationship between their ripening process and ethylene production suggested that both of them underwent a climacteric ripening process. However, the two cultivars expressed this character differentially. The climacteric trait of jujube may be related to the specific cultivar, according to the maturity stage. Consequently, differentiated postharvest management should be applied for cultivars P3 and P5 in order to maximize the shelf life and qualitative maintenance for the subsequent application. Moreover, the combination of ethylene production and biochemical characterization led us to identify some biochemical indicators of the ripening process, which could be used as physicochemical tools for sampling P3 and P5 fruits as raw material with a view to food processing. Acknowledgments Suzie Zozio was supported by a grant from Région Guadeloupe. This study was part of the African Food Tradition Revisited by Research (AFTER–http://www.after-fp7.eu/) research project funded by the European Union FP7 245-025. This research was supported by the European Regional Development Fund (ERDF) Convergence: Guadeloupe 2008-2013, PO Qualité des Produits Végétaux (Grant No. 1/1.4/32933 and 1/1.4/31612). The authors are grateful for the funding provided for this work. We would also like to thank Alexia Prades and Najat Talha, CIRAD Montpellier, for their support in the sugar analyses. References Abbas, M.E.F., 1997. Jujube. In: Mitra, K.S. (Ed.), Postharvest Physiology and Storage of Tropical and Subtropical fruits. CAB International, Wallingford, pp. 405–415. Abbas, M.E.F., Fandi, B.S., 2002. Respiration rate, ethylene production and biochemical changes during fruit development and maturation of jujube (Ziziphus mauritiana Lamk). J. Sci. Food Agric. 82 (13), 1472–1476. Al-Niami, J.H., Saggar, R.A.M., Abbas, M.E.F., 1992. The physiology of ripening of jujube fruit (Ziziphus mauritiana Lamk). Sci. Hortic. 51 (3–4), 303–308. Azam-Ali, S., Bonkoungou, E., Bowe, C., deKock, C., Godara, A., Williams, J.T., 2006. Ber and other jujubes (Ziziphus species). In: Fruits for the Future 2 – Revised Edition. University of Southampton. International Centre for Underutilised Crops, Southampton, UK. Bruno-Bonnet, C., Hubert, O., Mbéguié-A-Mbeguié, D., Pallet, D., Hiol, A., Reynes, M., Poucheret, P., 2013. Effect of physiological harvest stages on the composition of bioactive compounds in Cavendish bananas. JZhejiang Univ Sci. Zhejiang Univ. Sci. B 14 (4), 270–278. Chambroy, Y., Souty, M., Audergon, J.M., Jacquemin, G., Gomez, R.M., 1995. Researches on the suitability of modified atmosphere packaging for shelf-life and quality improvement of apricot fruit. Acta Hortic. 384, 633–638. Dadzie, B.K., Orchard, J.E., 1997. Evaluation post-récolte des hybrides de bananiers et bananiers plantains: critères et méthodes. Guides techniques INIBAP, Montpellier France. Gibert, O., Dufour, D., Reynes, M., Prades, A., Moreno Alzate, L., Giraldo, A., Escobar, A., González, A., 2013. Physicochemical and functional differentiation of dessert and cooking banana during ripening – a key for understanding consumer preferences. In: ISHS (Ed.), International ISHS-ProMusa Symposium on Bananas and Plantains: Towards Sustainable Global Production and Improved Use. Acta Horticulturae 986, Salvador (Bahia), Brazil, pp. 269–286. Gupta, R.B., Sharma, S., Sharma, J.R., Goyal, R., 2004. Study on the physico-chemical characters of fruits of some wild and cultivated forms/spp. (ziziphus spp.). Haryana J. Hort. Sci. 33 (3–4), 167–169. Jiang, W., Sheng, Q., Jiang, Y., Zhou, X., 2003. Effects of 1-methylcyclopropene and gibberellic acid on ripening of Chinese jujube (Zizyphus jujuba M) in relation to quality. J. Sci. Food Agric. 84, 31–34. Kaur, N., Aulakh, P.S., Arora, P.K., 2008. Physico-chemical characters as indices of maturity in Ber cultivars. Environ. Ecol. 26 (4A), 1746–1748. Lal, G., 2005. Effect of fruit harvesting time on post-harvest behaviour of Ber (Zyziphus mauritiana Lamk) cv. Umran. J. Res. ANGRAU 33 (4), 117–119. Lebellec, F., Lebellec, V., 2007. In: Orphie (Ed.), Le verger tropical: Cultiver les arbres fruitiers. Chevagny sur Guye, France, ISBN 10:2877633845. Meena, H.R., Kingsly, A.R.P., Jaln, R.K., 2009. Physical and mechanical properties of different Ber cultivars. Indian J. Hortic. 66, 261–263.
S. Zozio et al. / Scientia Horticulturae 175 (2014) 290–297 Mertz, C., Brat, P., Caris-Veyrat, C., Gunata, Z., 2010. Characterization and thermal lability of carotenoids and vitamin C of tamarillo fruit (Solanum betaceum Cav). Food Chem. 119 (2), 653–659. Pareek, S., Kitinoja, L., Kaushik, R.A., Paliwal, R., 2009. Postharvest physiology and storage of Ber. Stewart Postharvest Rev. 5 (5). Qiuping, Z., Wenshui, X., 2007. Effect of 1-methylcyclopropene and/or chitosan coating treatments on storage life and quality maintenance of Indian jujube fruit. LWT – Food Sci. Technol. 40 (3), 404–411. Sharma, R.K., Siddiqui, S., Gupta, O.P., 2000. Changes in ethylene evolution and respiration rates in ripening Ber (Zizyphus mauritiana Lamk) fruits while attached to or after being detached from the trees. Haryana J. Hortic. Sci. 29, 195–196.
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Sheng, J., Yunbo, L., Lin, S., 2003. Storage of Chinese winter jujube fruit. Acta Hortic. ISHS 620, 203–208. Sisler, E.C., Serek, M., 1997. Inhibitors of ethylene responses in plants at the receptor level: recent developments. Physiol. Plantrum 100, 577–582. Zhang, G.D., Feng, M., Yang, D., Liu, G.H., Yu, X.Y., Xu, W.P., 2009. Primary study on respiration type of Lingwu Changzao (Ziziphus jujube Mill.). Acta Hortic. ISHS 840, 483–488. Zozio, S., Servent, A., Cazal, G., Mbéguié-A-Mbéguié, D., Ravion, S., Pallet, D., Hiol, A., 2013. Changes in antioxidant activity during the ripening of jujube (Ziziphus mauritiana Lamk). Food Chem. 150, 448–456.
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Physicochemical and biochemical characterization of ripening in jujube (Ziziphus mauritiana Lamk) fruits from two accessions grown in Guadeloupe S. Zozio a,b , A. Servent b , O. Hubert a,b , A. Hiol c , D. Pallet b , D. Mbéguié-A-Mbéguié a,b,∗ a
CIRAD, UMR QUALISUD, F-97130 Capesterre-Belle-Eau, Guadeloupe, France CIRAD, UMR QUALISUD, F-34398 Montpellier, France c CIRAD, UMR QUALISUD Université de la Réunion – ESIROI, Spécialité agroalimentaire, PTU 97490 St Clotilde, France b
a r t i c l e
i n f o
Article history: Received 18 March 2014 Received in revised form 11 June 2014 Accepted 12 June 2014 Available online 11 July 2014 Keywords: Ethylene production Fruit ripening Jujube Ziziphus mauritiana
a b s t r a c t Jujube fruits (Ziziphus mauritiana Lamk) from two accessions grown in Guadeloupe were harvested and sampled at five ripening stages, from green to reddish-brown in colour. Their physiological characteristics were then investigated. Ascorbic acid increased with ripening until stage 4, to 463 mg/100 g and 168 mg/100 g dry weight, for cultivars P3 and P5, respectively. Likewise, ethylene production increased until stage 4, to 121 l/kg/h and 116 l/kg/h, for cultivars P3 and P5, respectively. High and transient sucrose accumulation was observed during ripening of P3 fruits, concomitantly with low and constant glucose and fructose contents. P5 fruits also accumulated sucrose transiently but at a lower level than P3 fruits, with a marked decrease at the end of ripening. In contrast to P3 fruit, glucose and fructose accumulated continuously to high levels during P5 fruit ripening. These data suggested differential sucrose metabolism during ripening of these fruits. Postharvest treatments with 1-MCP and acetylene were also performed on the three first ripening stages of both cultivars P3 and P5. On the basis of the findings, we discuss the climacteric behaviour of the P3 and P5 ripening process. © 2014 Elsevier B.V. All rights reserved.
1. Introduction Jujube (Ziziphus mauritiana Lamk), commonly known as “pomme-surette” in Guadeloupe, is widely distributed in the southern and northern parts of the island. The jujube tree, which belongs to the Ziziphus genus and the Rhamanceae family, is widespread throughout tropical and subtropical regions of Asia, Africa and Australia. Two major Ziziphus species are domesticated: Ziziphus mauritiana Lamk., the Indian jujube which is commonly known as Ber, and Ziziphus jujuba Miller, the Chinese jujube (Azam-Ali et al., 2006). Depending on the ripening stage, the jujube fruit peel colour shifts from green to yellow, and then from a reddish to brown colour. Generally, the fruit is eaten fresh and has a mild bittersweet flavour. Jujube is considered a functional fruit due to its high
∗ Corresponding author at: CIRAD, UMR QUALISUD, F-97130 Capesterre-BelleEau, Guadeloupe, France. Tel.: +590 590 86 17 70; fax: +590 590 86 80 77. E-mail addresses: [email protected] (S. Zozio), [email protected] (A. Servent), [email protected] (O. Hubert), [email protected] (A. Hiol), [email protected] (D. Pallet), [email protected], [email protected] (D. Mbéguié-A-Mbéguié). http://dx.doi.org/10.1016/j.scienta.2014.06.014 0304-4238/© 2014 Elsevier B.V. All rights reserved.
nutritional value. However, the shelf-life of jujube fruits is short (2–4 days at ambient temperature) and its rapid perishability was reported to be problematic for fruit postharvest management and advance processing (Pareek et al., 2009). The fruit quality traits depend on how the physiological development and ripening process occurs in the field and after harvesting. Consequently, characterizing this process and gaining further insight into the related physiological basis are essential prerequisites with a view to postharvest management and improving the fruit quality. Nevertheless, and in contrast to the Chinese jujube (Ziziphus jujuba Miller), only a few studies have been devoted to the Ziziphus mauritiana Lamk ripening process. The putative variability of the ripening process within the Ziziphus species has thus yet to be determined. With regard to their ripening behaviour, the few studies performed within the Ziziphus species, based on the ethylene production and respiration rate, suggested that Z. mauritiana and Z. spina-christi (L.), i.e. a wild native Iraqi species, exhibited climacteric ripening (Abbas and Fandi, 2002; Sharma et al., 2000), whereas Z. jujuba was recognized as being non-climacteric (Sheng et al., 2003; Zhang et al., 2009). The number of edible fruits in Guadeloupe has been estimated as up to 130, with high variability (Lebellec and Lebellec, 2007).
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However, heritage fruit of Guadeloupe has not been markedly promoted, apart from banana which is mainly grown for export. In order to promote this heritage fruit, we attempted to gain further insight into the quality properties of jujube (Ziziphus spp.), in order to investigate the potential value of this fruit as a fresh and/or processed product. Several of jujube fruit plots were identified in Guadeloupe, indicating that these fruits were exploited in the past by the island’s inhabitants. In this study, we physico-chemically characterized the ripening process of jujube fruit from two different accessions growing side by side in Guadeloupe. In addition to the ethylene and respiration criteria considered in previous studies, we combined postharvest 1-MCP, a well known ethylene binding inhibitor (Sisler and Serek, 1997), and acetylene, together with biochemical changes, to assess the ripening behaviour of the respective ripening process. The data obtained were further discussed in regard to the contrasted morphological features, including colour, firmness or size and nutritional attributes of these fruits, as highlighted previously (Zozio et al., 2013). 2. Materials and methods 2.1. Plant material 2.1.1. Fruit harvest for in planta analysis Two jujube fruit trees (Ziziphus mauritiana Lamk), identified as P3 and P5, that were at least 30 years old according to the farmers, were chosen based on the basis of their morphological features and global fruit taste. The P3 tree yielded sweet oblong fruit, while the P5 tree had bitter round fruit (Fig. 1). Fruits were harvested from each tree between January and February, corresponding to their optimal fructification period. Because of their desynchronized flowering and fruit development and ripening in planta, fruits of each tree were harvested manually by shaking the tree, on the same day, and sampled into five development stages according to their colour and size (Fig. 1). Some of the fruits were used to measure ethylene production, colour, size and firmness. Others were freezedried and kept under vacuum until use for biochemical analyses. 2.1.2. Fruit harvest for the postharvest investigation Based on the sampling described above, the first three ripening stages were chosen to study off-tree ripening in air at 20 ◦ C, and after postharvest treatment with 1-MCP and acetylene. 2.1.3. Post-harvest treatment Fruits sampled at the three first developmental stages were treated separately with 1000 ppm of acetylene and 0.5 ppm of 1MCP. The treatment was performed for 24 h at 20 ◦ C using a 35-l Plexiglas container. 1-MCP was prepared from a commercial powder provided by RHOM HASS (Pont Du Casse, France) according to the manufacturer’s instructions. Untreated fruits used as control were stored simultaneously in air under the same conditions. After acetylene- and 1-MCP treatments, fruits were kept to in a ripening chamber at 20 ◦ C. A sample of each treated fruit, and controls, were picked daily until the fruits reached the end of maturation (=0 l/kg/h of ethylene production) which was 6 and 7 days for P3 and P5, respectively. At this stage, the fruit samples were then freeze-dried for the sugar and organic acid analyses. 2.2. Physicochemical analysis 2.2.1. Ethylene measurement Ethylene production was measured during in planta and ex planta ripening according to the method described by (Chambroy et al., 1995). Approximately 30 fruits from each ripening stage were sealed in a 1–2 l glass container for 1 h at 20 ◦ C. A 100 l gas sample was withdrawn from the headspace using a gas-tight
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hypodermic syringe (Interchim, Montluc¸on, France) and analyzed using a CP-3800 gas chromatograph (Varian, Courtaboeuf, France) equipped with a flame ionization detector. Gas analysis was performed on a capillary PLOT fused silica column 25 m × 0.53 mm (Varian, Courtabeauf, France) under the following conditions: oven temperature 40 ◦ C, FID dectector temperature 150 ◦ C, helium as gas carrier (30 ml/min) and make up (20 ml/min), hydrogen at 4.5 bar and air at 300 ml/min. Ethylene concentrations were calculated from the calibration ethylene standard curve, and the results are expressed as l/kg/h. Experiments were performed on three biological replicates.
2.2.2. Firmness, colour and fruit size: in planta measurements Fruit firmness was measured in the equatorial region using a TAXT2 penetrometer (Swantec, Gennevilliers, France) and peel colour was measured as described by Bruno-Bonnet et al. (2013). The hue angle value (h◦ ) was used to assess the colour change with bluishgreen at 180◦ , yellow at 90◦ , and red-purple at an angle of 0◦ . The peel colour was measured at the apex of 15 fruits. Fruit size was measured on about 30 fruits from each ripening stage, as described by Dadzie and Orchard (1997), using a Vernier calliper (Mitutoyo, Roissy, France).
2.3. Biochemical analysis of in planta and ex planta fruit ripening after postharvest treatment 2.3.1. Organic acid determination Organic acids were extracted with H2 SO4 2.5 mM using a ratio of 0.5 g of dry matter to 10 mL of sulfuric acid. The mixture was agitated for 20 min with a Reax 2 shaker (Heidolph, Schwabach, Germany), then centrifuged for 10 min at 3300 × g (10 ◦ C) using a 5810R Eppendorf centrifuge (Le Pecq, France). HPLC analysis was performed on Agilent System 1200 series HPLC (Agilent 1200 HPLC system, Massy, France) using an HyperREZTM XP Carbohydrate Column H+ Ion Counter, 8 m, 8% cross linkage, 7.7 × 300 mm (ThermoScientific, Rochester, USA) with 0.05 M H2 SO4 as mobile phase at a 0.8 ml/min flow rate. The acids were identified by comparison of their retention times with standard (Supelco, Bellefonte, USA).
2.3.2. Sugar determination Soluble sugars were separated by high performance ionic chromatography (HPIC) as described by Gibert et al. (2013).
2.3.3. Ascorbic acid (AA) content Ascorbic acid content was assessed using the method of Mertz et al. (2010) with some modifications. Ascorbic acid was analyzed using an Agilent System 1200 series HPLC (Massy, France) with a ZORBAX Eclipse Plus C18 column (5 m, 4.5 × 250 mm, Agilent, Massy, France). The operating conditions were as follows: isocratic solvent system using a 0.01% solution of H2 SO4 at a 1 mL/min flow rate, 20 L injection volume, and detection was set at 245 nm. Extractions and analysis were carried out in triplicate. Ascorbic acid was quantified by external standard calibration. The results are expressed in mg AAS /100 g.
2.4. Statistical analysis The data were subjected to analysis of variance (ANOVA) using Statistica software (Statsoft, version 7). The means were separated by Duncan’s multiple range test (p < 0.05). Analyses were performed on three biological replicates.
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Fig. 1. Morphological features of jujube fruits from P3 and P5 accessions grown in Guadeloupe. Jujube fruits were harvested from plants grown on a local farm based in the southern part of the island and under natural conditions. Then they were grouped according to their colour and form.
3. Results 3.1. Physicochemical and biochemical changes during in planta ripening Physicochemical changes during jujube fruit were assessed through ethylene production, colour firmness and fruit diameter measurement (Table 1). The level of ethylene production increased transiently, with a peak at 121.46 ± 1.55 l/kg/h for cultivar P3, and 116.75 ± 2.18 l/L/kg/h for cultivar P5. Interestingly, both reached the peak at stage 4, and then the production decreased sharply. At the first harvest stage, the hue value was 114◦ ± 1.55 and 112◦ ± 2.67 for cultivars P3 and P5, respectively. A significant decrease in hue value was observed between ripening stages 3 and 4 for cultivar P3 (20%), and between stages 2 and 3 for cultivar P5 (33%) (p < 0.05). At the late ripening stage, fruits of both cultivars exhibited a comparable hue value (65◦ and 67◦ ) (Table 1). Concerning the fruit firmness, cultivars P3 and P5 exhibited a differential softening pattern during ripening. Cultivar P3 remained firmer during ripening, while the firmness in P5 fruits began to decrease drastically by 67% (11.89 N ± 1.39–4.37 N ± 0.71 p < 0.05) at stage 3 (Table 1). For both cultivars P3 and P5, fruit size increased slightly at a comparable level during in planta ripening. At the late ripening stage, the size of both cultivar P3 and P5 fruits exhibited a comparable diameter of approximately 29 mm, which is in accordance with previously reported data (Gupta et al., 2004; Meena et al., 2009) (Table 1). Sugar content changes are described in Table 2. During in planta ripening of P3 fruit, sucrose accumulated to a maximum level reached at stage 4, before decreasing slightly to 30% at stage 5, as also reported by Abbas and Fandi (2002). The sucrose level was 5- and 7-fold higher than the glucose and fructose levels, respectively. However, no marked changes were observed in glucose and fructose levels throughout ripening. For P5 fruit, the sucrose accumulation pattern was similar but at a lower level, with a drastic decrease (92%) at ripening stage 5. At this stage, P5 fruit accumulated 3-fold more glucose and fructose than P3. The ascorbic acid analysis revealed a significant and higher ascorbic acid content in cultivar P3 than in P5. Similar to the ethylene pattern, an increase in ascorbic acid was observed until the 4th stage for cultivars P3 and P5 (463.61 ± 13.93 and 258.78 ± 4.37 mg/100 g, respectively), and then a decrease was observed. The decrease in the hue angle observed in cultivar P3 and P5 was correlated with the ripening pattern (Table 2).
Malic acid was the most abundant of all the organic acids analyzed in both cultivars P3 and P5, while tartaric acid was the least abundant. Concerning the two major acid components, i.e. malic and citric acid, both accessions accumulated a comparable level of citric acid, whereas cultivar P5 exhibited a higher level of malic acid than cultivar P3 (25% for stage 1 and 60% for stage 5). For cultivars P3 and P5, the citric acid level decreased slightly from stage 1 to 5, while the tartaric acid level increased. Transient accumulation of malic acid was observed during the ripening of both P3 and P5 fruits, with a maximum observed at stage 2. 3.2. Effects of postharvest treatments on fruit ripening and related biochemical changes Postharvest ripening of P3 and P5 fruits was investigated in fruit sampled at the first three development stages. Fruits from each cultivar were treated with 1-MCP or acetylene, and left to ripen in air at 20 ◦ C until decay, which occurred at 6 days for cultivar P3 fruits and at 7 days for cultivar P5. Untreated fruits sampled at the same developmental stage were used as control. For each cultivar, postharvest ripening was monitored daily by measuring ethylene production at the same time. According to the developmental stages, postharvest treatments differentially affected the ethylene production of cultivar P3 and P5 fruits (Fig. 2). For fruit harvested at the 1st ripening stage, only acetylenetreated cultivar P5 fruits produced a higher level of ethylene than 1-MCP-treated and control fruits, from which the ethylene levels were comparable. However, no marked change was observed in cultivar P3 fruits, irrespective of the postharvest treatment (Fig. 2A and D). At the 2nd stage for cultivar P3, the ethylene level increased, regardless of the treatment, 24 h after treatment (Fig. 2B). A transient ethylene production peak was observed at 72 h for acetylene-treated and control fruits, while for 1-MCP-treated fruits, the peak was reached later at 96 h. Maximum ethylene production was higher in acetylene-treated fruits compared to control and 1-MCP-treated fruits. For cultivar P5, the ethylene production pattern was similar to that observed for fruits sampled at stage 1 (Fig. 2E). Ethylene production increased continuously regardless of the treatment. However, the ethylene level was higher with acetylene-treated fruits than for the 1-MCP-treated and control fruits. For fruits harvested at an advanced ripening stage (stage 3), cultivars P3 and P5 exhibited different ethylene production patterns.
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Storage me aer treatment (Hours)
E
B Control 1-MCP
120
Acethylene
0 a a a
24 a a b
48 72 a a b a b b
96 a b b
120 a b b
140 Ethylene producon (μl/Kg/h)
140 Ethylene producon (μl/Kg/h)
0 a a a
100
0
100 80 60 40 20
Control 1-MCP Acethylene
120 100
0 a a a
24 48 72 96 120 144 a a a a a a a b b b a a b b b c b b
80 60 40 20 0
0 0
24
48
72
96
24
0
120
48
Control 1-MCP Acethylene
140 120
0 a b b
24 a b c
48 a b a
72 a b a
96 a b a
120 a,b b a
100 80 60 40 20
0 Control a 1-MCP b Acethylene a
F 140 Ethylene producon (μl/Kg/h)
C
72
96
120
144
Storage me aer treatment (Hours)
Storage me aer treatment (Hours)
Ethylene producon (μl/Kg/h)
293
24 a a a
48 a a a
72 a a b
96 a a b
120 a a a
144 a a a
120 100 80 60 40 20 0
0 0
24
48
72
96
120
Storage me aer treatment (Hours)
0
24
48 72 96 120 Storage me aer treatment (Hours)
144
Fig. 2. Effects of postharvest treatment (1-MCP and acetylene) on ethylene production rates of P3 (A–C) and P5 (D–F) tree fruits harvested at stages 1 (A and D), 2 (B and E) and 3 (C and F). Fruits were exposed to 0 (control) or 0.5 ppm 1-MCP or 1000 ppm acetylene for 24 h, and then kept in air at 20 ◦ C and 80–90%. Each point represents the mean of three replicates ± SE. HT: harvest time. The table above each graph shows the significant difference during ripening for one treatment.
For cultivar P3, a similar ethylene production pattern was observed regardless of the treatment, with a transient ethylene production peak reached at 24 h for the control and acetylene-treated fruits, and at 48 h for 1-MCP treated fruits. For cultivar P5, the control and treated fruits exhibited a similar ethylene production pattern, with a transient peak at 48 h after treatment (Fig. 2F).
Remarkably, acetylene-treated P5 fruits reached an ethylene level at 72 h (119.7 ± 11.5 l/kg/h) similar to that of the stage 4 fruits harvested on the tree (116.7 ± 2.1 l/kg/h). However, the control reached only 94.3 ± 3.8 l/kg/h (Fig. 2F). Furthermore, this increase was not observed in treated P3 fruits.
294
Table 1 Ethylene production, ascorbic acid and some physical characteristics assessed during in planta ripening (stages 1–5) of jujube fruits from trees P3 and P5. The value in brackets is the standard deviation. Characteristics
Ripening stages in planta Cultivar P3
Ethylene production (l/kg/h) Skin hue angle (◦ ) Firmness (N) Fruit diameter (cm)
Cultivar P5
1
2
3
4
5
1
2
3
4
5
1.84 (0.26) 114.15 (1.55) 10.97 (1.80) 23.48 (1.61)
5.59 (0.14) 110.42 (2.53) 9.97 (1.32) 27.48 (2.20)
40.04 (5.48) 104.29 (3.73) 9.47 (1.63) 27.52 (1.56)
121.46 (1.55) 82.55 (4.62) 9.13 (1.52) 30.61 (2.13)
0.00 (0.00) 65.39 (2.35) 7.55 (1.21) 30.86 (2.06)
0.00 (0.00) 112.53 (2.67) 12.69 (1.06) 23.44 (1.00)
1.12 (0.07) 108.05 (2.20) 13.14 (1.51) 26.79 (1.71)
26.80 (1.23) 90.90 (2.04) 11.89 (1.39) 27.78 (1.96)
116.75 (2.18) 72.07 (4.96) 4.37 (0.71) 27.81 (2.72)
0.00 (0.00) 66.68 (3.81) 3.16 (0.58) 28.41 (2.09)
Table 2 Ascorbic acid (mg/100 g), organic acid (mg/g) and sugar (mg/g) contents after the maturation of P3 and P5 fruits sampled at the three first ripening stages and treated with 1-MCP and acetylene, and left in a maturation chamber at 20 ◦ C until the last ripening stage (5). Ripening stages in planta Cultivar P3
Ascorbic acid (mg/100 g) Organic acids (mg/g) Citric acid Tartaric acid Malic acid Sugars (mg/g) Glucose Fructose Sucrose
Cultivar P5
1
2
3
4
5
1
2
3
4
5
200.61 (10.92)
322.48 (3.10)
387.40 (3.11)
463.61 (13.93)
158.50 (1.12)
114.69 (1.35)
137.11 (0.91)
168.59 (30.20)
258.78 (4.37)
184.85 (0.10)
49.46 (2.14) 5.08 (0.59) 81.36 (3.42)
33.18 (5.44) 6.88 (1.87) 66.04 (3.09)
27.60 (4.25) 9.17 (1.48) 47.51 (4.94)
46.65 (5.00) 6.88 (1.50) 97.18 (7.00)
44.46 (7.00) 5.91 (1.22) 103.14 (7.00)
29.93 (3.00) 6.48 (1.60) 101.86 (7.50)
25.89 (6.68) 7.39 (1.23) 87.29 (9.71)
24.76 (7.76) 9.16 (1.48) 76.20 (6.24)
90.36 (1.11) 92.18 (0.75) 266.26 (4.30)
71.83 (1.49) 82.88 (0.41) 109.84 (4.13)
150.78 (12.70) 158.85 (12.05) 248.71 (6.29)
107.39 (2.28) 110.43 (3.36) 248.51 (4.67)
123.72 (7.94) 126.44 (7.65) 238.90 (7.14)
267.53 (5.82) 261.96 (6.24) 17.70 (0.85)
46.71 (5.27) 3.26 (1.31) 77.91 (5.12) 82.85 (0.92) 90.51 (0.66) 259.06 (4.62)
82.65 (2.86) 89.12 (3.65) 359.41 (20.83)
The italics characters correspond to standard deviation values.
76.78 (0.27) 81.60 (1.15) 383.98 (9.65)
30.86 (6.78) 8.58 (1.06) 60.70 (8.04) 78.94 (2.24) 80.44 (2.21) 386.69 (25.47)
S. Zozio et al. / Scientia Horticulturae 175 (2014) 290–297
The italics characters correspond to standard deviation values.
S. Zozio et al. / Scientia Horticulturae 175 (2014) 290–297
Tartaric Acid b
b a
a
a
a a
a
a
a
a
a
a a
a
a
b a
a a
b
b
b
a a
a
a
Sugar mg/g of DM
A
a
250
A
200
aa
a
sucrose
a aa
a bb
150
c
ba
c
b
a
a
b
100 50
a
b
b
0
2
3
1
Control
2
3
1
1-MCP Treatments
Citric acid Organic acids mg/g of DM
fructose
300
1
140 120 100 80 60 40 20 0
glucose
Malic Acid
Tartaric acid
2
3
1
a
300
b
a a
a
b b
a
a
a
a
b
b b
a
a
1
2
3
1
1-MCP
2
3
Acetylene
Treatments
Malic acid
a
3
Control
B a
2
Acetylene
a
a
a
a
a
a
a
a
a
1
2
3
1
2
3
1
2
3
Sugar mg/g of DM
Organic acid mg/g of DM
Citric Acid 140 120 100 80 60 40 20 0
295
250
glucose
B
200
fructose aa
aa a
150
a bb
aa
1
2
a b
b
aa
bb
a 100 50 0
Control
1-MCP
1
3
Control
Acetylene
3
1-MCP
1
2
3
Acetylene
Treatments
Treatments Fig. 3. Organic acid content in jujube fruits from cultivars P3 (A) and P5 (B) measured at the end of ex planta maturation at 20 ◦ C. Fruits were sampled at stages 1–3 for 24 h treatments with 1-MCP and acetylene, and then left in a maturation chamber for 6 days for P3 fruits and 7 days for P5 fruits. The control represents untreated fruits. The values are expressed in mg of acid per g of dry matter. Different letters (a, b, c) express the significant effect of treatment (1-MCP and acetylene vs. control) for one ripening stage using Duncan’s multiple range test at p < 0.05.
2
Fig. 4. Content of sugars identified in jujube fruits from cultivars P3 (A) and P5 (B) measured at the end of ex planta maturation at 20 ◦ C. Fruits were sampled at stages 1–3 for 24 h treatments with 1-MCP and acetylene, and then left in a maturation chamber for 6 days for P5 fruits and 7 days for P5 fruits. The control represents untreated fruits. The values are expressed in mg of sugar per g of dry matter. Different letters (a, b, c) express the significant effect of treatment (1-MCP and acetylene vs. control) for one ripening stage using Duncan’s multiple range test at p < 0.05.
4. Discussion The sugar as well as organic acid per dry matter levels was also measured in order to check the biochemical changes during ripening of P3 and P5 jujube fruit. Accumulation in control fruits showed that their level was differentially affected by the postharvest storage conditions described in this study, according to the fruit physiological stage at harvest and the accession (Figs. 3 and 4). For all P3 and P5 fruits tested, compared to their physiological stage at harvest, postharvest storage increased by up to 2-fold the tartaric acid level, and up to 2–3-fold the glucose and fructose level (2–3-fold each). For P3 fruits, the malic acid level decreased slightly (up to 1.4-fold) for P3 fruits at all physiological stages while, for P5 fruits, this decrease was observed only in fruits sampled at stage 3. For both P3 and P5 fruits, the postharvest storage conditions induced a drastic decrease in sucrose content (up to 36-fold for P3), while no trace was detected in P5 fruits. Citric acid accumulation varied according to the physiological stage at harvest. For fruit sampled at the first physiological stage, the postharvest storage conditions increased the citric acid level by 1.2-fold only at stage 1 for P3, and at stages 1 and 2 for P5 fruits, respectively. The effect of acetylene and 1-MCP on the biochemical content was also investigated in this study. As compared to the controls (untreated fruits), no marked changes were observed in all other biochemical contents in acetylene and 1-MCP treated fruits, except for citric acid in P5 fruits. Acetylene-treated fruits exhibited a higher citric acid level (1.5-fold on average) than 1-MCP treated fruits, whose citrate content was comparable to that of the controls.
In this study, we carried out physicochemical and biochemical characterizations of the ripening process in jujube fruits from two accession trees, with contrasting morphological features, grown in Guadeloupe. During in planta ripening, both P3 and P5 fruits exhibited a similar ethylene production pattern characterized by a transient ethylene peak at stage 4, in agreement with previously reported data (Abbas and Fandi, 2002; Al-Niami et al., 1992; Lal, 2005; Kaur et al., 2008; Qiuping and Wenshui, 2007; Sharma et al., 2000). However, contrasted patterns were noted in terms of softening, with P3 fruits being firmer during ripening than P5 fruits. Moreover, during their respective in planta ripening processes and compared to P5 fruit, P3 fruits accumulated on average 2-fold more ascorbic acid and sucrose. The ascorbic acid content and sucrose/(glucose + fructose) ratio, primarily due to the sucrose content, could thus be considered as a biochemical indicator of P3 and P5 fruit ripening. Taken together, our data indicated that the various morphological features of the P3 and P5 accessions were also reflected in the fruit ripening process and the corresponding biochemical changes. Considering that the P3 and P5 accessions had been planted more than 30 years earlier and had been growing in the same agroclimatic region, our data suggest that the P3 and P5 accessions were probably different Z. mauritiana cultivars. However, it would be interesting to confirm this hypothesis through genetic diversity analysis. With regard to the climacteric behaviour of the jujube fruit ripening process, previous studies reported contrasting data on the general trend, ascribing the climacteric nature to a concomitant respiration crisis with a burst of ethylene synthesis. Abbas and
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Fandi (2002) reported climacteric behaviour in the Z. mauritiana cultivar Zaytoni, while Sheng et al. (2003) and Zhang et al. (2009) reported non-climacteric behaviour in Zizyphus jujuba. However, the climacteric features of Zizyphus fruit cannot be clearly related to the species, as the Zizyphus jujuba Jing cultivar is reported to exhibit climacteric ripening 1 behaviour (Jiang et al., 2003). To assess the climacteric behaviour of P3 and P5 accession fruits, we examined the ethylene production of both P3 and P5 fruits sampled at different developmental stages and treated with acetylene (an ethylene analogue) and 1-MCP, an inhibitor of ethylene action (Sisler and Serek, 1997). Our data suggested that the ripening process of jujube fruit from P3 and P5 accessions undergoes climacteric behaviour in different ways. Ethylene production of cultivars P3 and P5 fruits was affected differentially by acetylene and 1-MCP, according to the developmental stage, thus supporting the hypothesis that the P3 and P5 accessions are probably different cultivars. For P3 accession fruits, 1-MCP treatment induced a delay in ethylene production during postharvest ripening at stages 2 and 3 as compared to acetylene-treated and control fruits. At stage 2, acetylene treatment increased fruit ethylene production, which reached an early peak (72 h after treatment), while that of 1-MCP treated fruits was obtained later (96 h after treatment). At stage 3, a transient ethylene peak was reached earlier in control and acetylene-treated fruits than in 1-MCP treated fruits. These data suggested that P3 fruits exhibited climacteric behaviour. Surprisingly, when harvested at an earlier developmental (stage 1), P3 fruits treated with acetylene and 1-MCP produced ethylene at comparable levels, higher than the control, with a similar pattern. We could not explain this atypical ethylene production pattern. The P5 accession of jujube fruit exhibited climacteric behaviour earlier, since the antagonistic effect of 1-MCP and acetylene was first observed at stage 1, and was exacerbated at stage 2. In contrast, at stage 3, the antagonistic effect of 1-MCP and acetylene on ethylene production was less marked between treatments than in fruit harvested at stages 1 and 2. The ethylene responsiveness of the fruit might have been complete enough to be affected by our 1-MCP treatments. Note also that under our postharvest conditions, and regardless of the developmental stage at harvest, the decrease in ethylene production used here as a physiological indicator of the late ripening stage occurred at 6 and 7 days for P3 and P5 fruits, respectively. Al-Niami et al. (1992) reported a similar storage life for two other jujube varieties. As compared to the control fruit, these data indicated that the level of ethylene fruit responsiveness at harvest impacts the level of fruit ethylene production during postharvest storage, as discussed previously, while not affecting the fruit storage life. Previous studies showed a drastic decline in respiration rate at the end of storage life, suggesting a putative relationship between respiration and storage life duration (Abbas, 1997; Al-Niami et al., 1992). We are, however, unable to discuss this hypothesis here due to the lack of jujube fruit respiration data in this study, as well as the insufficient data on the organic acid compound related to respiration (i.e. malate). Postharvest storage, acetylene and 1-MCP treatment also differentially affected other biochemical compounds in P3 and P5 fruits. Our postharvest storage conditions induced the accumulation of some biochemical compounds, including glucose, fructose and tartaric acid, while others such as sucrose were completely eliminated. Neither ethylene nor 1-MCP affected the sugar and tartaric acid content in P3 and P5 fruit, citric acid in P3 fruit or malic acid in P5 fruit, suggesting that the metabolism of these components are under ethylene independent regulation. We failed to explain the rise in malic acid content in acetylene- and 1-MCP-treated P3 fruits to a similar level as in the controls. In contrast, citric acid, whose content was induced in P5 acetylene-treated fruit as compared to control and 1-MCP-treated fruits, is probably positively regulated by ethylene in this accession.
5. Conclusion In this study, we characterized jujube fruit from two accession trees (P3 and P5) grown in Guadeloupe. Our data led us to conclude that these two accessions were probably two different cultivars. The study of the relationship between their ripening process and ethylene production suggested that both of them underwent a climacteric ripening process. However, the two cultivars expressed this character differentially. The climacteric trait of jujube may be related to the specific cultivar, according to the maturity stage. Consequently, differentiated postharvest management should be applied for cultivars P3 and P5 in order to maximize the shelf life and qualitative maintenance for the subsequent application. Moreover, the combination of ethylene production and biochemical characterization led us to identify some biochemical indicators of the ripening process, which could be used as physicochemical tools for sampling P3 and P5 fruits as raw material with a view to food processing. Acknowledgments Suzie Zozio was supported by a grant from Région Guadeloupe. This study was part of the African Food Tradition Revisited by Research (AFTER–http://www.after-fp7.eu/) research project funded by the European Union FP7 245-025. This research was supported by the European Regional Development Fund (ERDF) Convergence: Guadeloupe 2008-2013, PO Qualité des Produits Végétaux (Grant No. 1/1.4/32933 and 1/1.4/31612). The authors are grateful for the funding provided for this work. We would also like to thank Alexia Prades and Najat Talha, CIRAD Montpellier, for their support in the sugar analyses. References Abbas, M.E.F., 1997. Jujube. In: Mitra, K.S. (Ed.), Postharvest Physiology and Storage of Tropical and Subtropical fruits. CAB International, Wallingford, pp. 405–415. Abbas, M.E.F., Fandi, B.S., 2002. Respiration rate, ethylene production and biochemical changes during fruit development and maturation of jujube (Ziziphus mauritiana Lamk). J. Sci. Food Agric. 82 (13), 1472–1476. Al-Niami, J.H., Saggar, R.A.M., Abbas, M.E.F., 1992. The physiology of ripening of jujube fruit (Ziziphus mauritiana Lamk). Sci. Hortic. 51 (3–4), 303–308. Azam-Ali, S., Bonkoungou, E., Bowe, C., deKock, C., Godara, A., Williams, J.T., 2006. Ber and other jujubes (Ziziphus species). In: Fruits for the Future 2 – Revised Edition. University of Southampton. International Centre for Underutilised Crops, Southampton, UK. Bruno-Bonnet, C., Hubert, O., Mbéguié-A-Mbeguié, D., Pallet, D., Hiol, A., Reynes, M., Poucheret, P., 2013. Effect of physiological harvest stages on the composition of bioactive compounds in Cavendish bananas. JZhejiang Univ Sci. Zhejiang Univ. Sci. B 14 (4), 270–278. Chambroy, Y., Souty, M., Audergon, J.M., Jacquemin, G., Gomez, R.M., 1995. Researches on the suitability of modified atmosphere packaging for shelf-life and quality improvement of apricot fruit. Acta Hortic. 384, 633–638. Dadzie, B.K., Orchard, J.E., 1997. Evaluation post-récolte des hybrides de bananiers et bananiers plantains: critères et méthodes. Guides techniques INIBAP, Montpellier France. Gibert, O., Dufour, D., Reynes, M., Prades, A., Moreno Alzate, L., Giraldo, A., Escobar, A., González, A., 2013. Physicochemical and functional differentiation of dessert and cooking banana during ripening – a key for understanding consumer preferences. In: ISHS (Ed.), International ISHS-ProMusa Symposium on Bananas and Plantains: Towards Sustainable Global Production and Improved Use. Acta Horticulturae 986, Salvador (Bahia), Brazil, pp. 269–286. Gupta, R.B., Sharma, S., Sharma, J.R., Goyal, R., 2004. Study on the physico-chemical characters of fruits of some wild and cultivated forms/spp. (ziziphus spp.). Haryana J. Hort. Sci. 33 (3–4), 167–169. Jiang, W., Sheng, Q., Jiang, Y., Zhou, X., 2003. Effects of 1-methylcyclopropene and gibberellic acid on ripening of Chinese jujube (Zizyphus jujuba M) in relation to quality. J. Sci. Food Agric. 84, 31–34. Kaur, N., Aulakh, P.S., Arora, P.K., 2008. Physico-chemical characters as indices of maturity in Ber cultivars. Environ. Ecol. 26 (4A), 1746–1748. Lal, G., 2005. Effect of fruit harvesting time on post-harvest behaviour of Ber (Zyziphus mauritiana Lamk) cv. Umran. J. Res. ANGRAU 33 (4), 117–119. Lebellec, F., Lebellec, V., 2007. In: Orphie (Ed.), Le verger tropical: Cultiver les arbres fruitiers. Chevagny sur Guye, France, ISBN 10:2877633845. Meena, H.R., Kingsly, A.R.P., Jaln, R.K., 2009. Physical and mechanical properties of different Ber cultivars. Indian J. Hortic. 66, 261–263.
S. Zozio et al. / Scientia Horticulturae 175 (2014) 290–297 Mertz, C., Brat, P., Caris-Veyrat, C., Gunata, Z., 2010. Characterization and thermal lability of carotenoids and vitamin C of tamarillo fruit (Solanum betaceum Cav). Food Chem. 119 (2), 653–659. Pareek, S., Kitinoja, L., Kaushik, R.A., Paliwal, R., 2009. Postharvest physiology and storage of Ber. Stewart Postharvest Rev. 5 (5). Qiuping, Z., Wenshui, X., 2007. Effect of 1-methylcyclopropene and/or chitosan coating treatments on storage life and quality maintenance of Indian jujube fruit. LWT – Food Sci. Technol. 40 (3), 404–411. Sharma, R.K., Siddiqui, S., Gupta, O.P., 2000. Changes in ethylene evolution and respiration rates in ripening Ber (Zizyphus mauritiana Lamk) fruits while attached to or after being detached from the trees. Haryana J. Hortic. Sci. 29, 195–196.
297
Sheng, J., Yunbo, L., Lin, S., 2003. Storage of Chinese winter jujube fruit. Acta Hortic. ISHS 620, 203–208. Sisler, E.C., Serek, M., 1997. Inhibitors of ethylene responses in plants at the receptor level: recent developments. Physiol. Plantrum 100, 577–582. Zhang, G.D., Feng, M., Yang, D., Liu, G.H., Yu, X.Y., Xu, W.P., 2009. Primary study on respiration type of Lingwu Changzao (Ziziphus jujube Mill.). Acta Hortic. ISHS 840, 483–488. Zozio, S., Servent, A., Cazal, G., Mbéguié-A-Mbéguié, D., Ravion, S., Pallet, D., Hiol, A., 2013. Changes in antioxidant activity during the ripening of jujube (Ziziphus mauritiana Lamk). Food Chem. 150, 448–456.