Impact of low oxygen storage on quality attributes including pigments and volatile compounds in ‘Shelly’ mango

Scientia Horticulturae 250 (2019) 174–183

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Impact of low oxygen storage on quality attributes including pigments and volatile compounds in ‘Shelly’ mango

T

Makgafele Lucia Ntsoanea,b, Alexandru Lucac, Manuela Zude-Sassea, Dharini Sivakumarb, ⁎ Pramod V. Mahajana, a

Department of Horticultural Engineering, Leibniz Institute for Agricultural Engineering and Bioeconomy (ATB), Potsdam, Germany Phytochemical Food network research group, Department of Crop Sciences, Tshwane University of Technology (TUT), Pretoria West, South Africa c Department of Food Science, Aarhus University, Årslev, Denmark b

A R T I C LE I N FO

A B S T R A C T

Keywords: Controlled atmosphere storage Low oxygen limit Mango Pigments Volatile organic compounds

Optimal oxygen conditions in controlled atmosphere storage play an important role in maintaining quality and extending shelf life of mangoes, especially for long distance markets. The aim of the study was to investigate the low O2 tolerance limit of 'Shelly' mango fruit based on quality attributes including pigments and accumulation of O2 restricted volatile organic compounds (VOCs). Spectroscopy in the visible wavelength range was applied in diffuse reflectance mode as a non-destructive method for monitoring the pigment contents. Furthermore, the relationship between non-destructively measured pigment indices and pigment content was investigated. The spectral reflectance measurements predicted the pigment content in mango fruit (R2 ≥ 0.70). However, experimental results showed that low O2 had no impact on pigment contents. Soluble solids and individual sugars (sucrose, fructose, and glucose) increased in all storage conditions. Significant differences were found in VOCs, 1% O2 resulted in significant accumulation of anaerobic metabolites: ethanol, ethyl acetate, 3-hydroxy-2-butanone, ethyl butanoate, 1-butanol, 2, 3-butanediol, ethyl propanoate, 2, 3-butanediol, undecane. Sensory analysis indicated that the panelists rejected fruit stored at 1% O2 due to unfavorable odour and taste. The results showed that 5% is the low O2 limit for 'Shelly' mango, below which anaerobic metabolites accumulated compromising the acceptability of the fruit due to ‘off-flavour’. However, storage conditions of 10% O2 can already result in reduced fruit mass loss and respiration rate; maintained the fruit flesh firmness, soluble solids content, and individual sugars in ‘Shelly’ mango after 21 d of storage.

1. Introduction Mango (Mangifera indica L.) is one of the most economically important tropical fruit worldwide in terms of production, consumption (attractive aroma and flavour) and nutritional value (Singh et al., 2013). Mango fruit can be considered as a rich source of health promoting compounds including vitamin C, β-carotene and polyphenols, that contribute towards antioxidant and nutritional properties (Sivakumar et al., 2011). However, climacteric mango fruit undergoes physiological and compositional changes during ripening which may result in rapid occurrence of postharvest losses (Lalel and Singh, 2004). Therefore, limited storage life of the mango fruit is the major constrain, particularly, when exporting mangoes to distant overseas markets (Sivakumar et al., 2011). During ripening the mango fruit undergoes remarkable changes in pulp and, in some cultivars, peel colour, shifting from green to yellow-orange as a result of changes in content and

⁎

composition of individual pigments. The changes in colour are related to chlorophyll degradation and biosynthesis of carotenoids, and, in some cultivars, anthocyanins in the peel (Seifert et al., 2014; Rungpichayapichet et al., 2015). Marketability of mango fruit depends on fruit colour appearance, as said, determined by pigment contents, which is an important quality component, but also being potentially a maturity indicator (Nordey et al., 2014). Furthermore, carotenoids content of ripe mango fruit are a good source of provitamin A and can be a nutritional source for malnourished people (Rungpichayapichet et al., 2015). Fruit pigments can be measured using non-destructive methods such as reflectance spectroscopy (Zude, 2003; Pflanz and Zude, 2008; Zude et al., 2007; Nordey et al., 2014) and using handheld spectrophotometers measuring in the visible wavelength range (Seifert et al., 2014; Marques et al., 2016). Non-destructive reflectance measurements in the wavelength range of 400–800 nm have been suggested to predict the main pigment content

Corresponding author. E-mail address: [email protected] (P.V. Mahajan).

https://doi.org/10.1016/j.scienta.2019.02.041 Received 10 August 2018; Received in revised form 12 February 2019; Accepted 13 February 2019 0304-4238/ © 2019 Elsevier B.V. All rights reserved.

Scientia Horticulturae 250 (2019) 174–183

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flushed when necessary to maintain the desired storage conditions. The changes of O2 and CO2 concentrations were monitored daily for a storage period of 21 d using gas analyser (Checkmate 3, PBI Dansensor, Ringstead, Denmark). After storage for 21 d at 13 °C, fruits were subjected to market shelf condition for 7 d at 18 °C under normal air. Chambers were opened once a week for sampling fruit analyzed further.

in fruit and vegetables: chlorophyll a and b, carotenoids, and anthocyanin. However, limited information has been published for use of non-destructive reflectance measurements for analyzing pigments of mango and no information has been reported for 'Shelly' mango to our knowledge. To extend the storage life of mango fruit with acceptable quality, various postharvest treatments have been investigated over last decades. These approaches involve the alteration of the natural conditions of the fruit to prolong its postharvest shelf life, preserve nutritional compounds and maintain sensory quality. This include, heat treatment (Anwar and Malik, 2007), cold storage management, 1-methylcyclopropen (1-MCP) (Sivakumar et al., 2012), ethylene (Montalvo et al., 2007), methyl jasmonate (González-Aguilar et al., 2000), edible coatings (Vázquez-Celestino et al., 2016) and controlled atmosphere (CA) storage (Sudhakar Rao and Gopalakrishna Rao, 2008). The use of CA and particularly low oxygen (O2) during storage of mango fruits has been investigated over the last decades as low O2 is reported to result in reduced rates of ethylene production, respiration, fruit softening, formation of flavour, chlorophyll degradation, and loss of organic acids (Sudhakar Rao and Gopalakrishna Rao, 2008). Hence, to determine low O2 limit (LOL) in CA storage for various mango cultivars to maintain the quality attributes and prolong the shelf life of mango fruit is essential. The recommended and commonly used CA storage atmospheres for extending mango shelf-life are 3–5% O2 and 5–10% carbon dioxide (CO2) (Kader, 1994; Yahia, 2009, 1998b). Storage under extremely low O2 conditions of < 2%, may result in anaerobic respiration and development of ‘off-flavours’, fruit discolouration, irregular ripening and increased susceptibility to decay (Singh and Zaharah, 2015). However, different outcomes have been reported in literature as previous studies demonstrated that there are cultivar differences in terms of CA conditions. Some cultivars can tolerate higher CO2 levels and levels of O2 lower than 2% (Bender et al., 2000). However, an extremely low O2 condition is reported to cause damage to the quality of fruit and vegetables by off-flavours (Nakamura et al., 2004). Fruit stored in CA storage of 1.5% O2 + 6% CO2, or in 1.5% or 2% O2 + 8% CO2 were reported to produce alcohol (ethanol), acetaldehyde, and esters in 'R2E2′ mangoes (Lalel and Singh, 2006). The objectives of the present work were (i) to recommend CA storage conditions for 'Shelly' mango, and particularly on LOL. (ii) To evaluate non-destructive analysis for monitoring fruit pigments applying chromatographic reference analyses. Furthermore, (iii) the characterization of volatile metabolites that accumulate in restricted O2 storage conditions was targeted.

2.2. Analyses of physicochemical properties 2.2.1. Gas exchange analyses Fruit respiration rate (RR) was measured using a closed system respirometer developed in-house (Rux et al., 2017a,b), consisting of 9 acrylic glass cuvettes (8.2 L) and each fitted with non-dispersive infrared CO2 sensor (GMP222, Vaisala GmbH, Bonn, Germany) with a measuring capacity of 0.1 × 10−3 to 5 g L-1 for 6 h (Rux et al., 2017a,b). For the measurement, fruits from each treatment were weighed and single fruit from each treatment was placed in separate cuvette and CO2 data was recorded every min. The RR was calculated when a constant increase of CO2 accumulation was measured and results were expressed as mg CO2 kg-1 h-1, with two replicates for each treatment. 2.2.2. Mass loss Fruit mass was recorded using an electronic balance (CPA10035, Sartorius, Göttingen, Germany). Consecutively every sampling day, the difference in mass was recorded and expressed in % mass loss (Caleb et al., 2016). Fruit substrate loss illustrated in Eq. (1) was calculated as glucose equivalents based on respiration rate. Six replicates were used for each treatment.

Substrate loss (Msub) = RR x

180 264

(1)

Where, Msub is the mass loss based on substrate, while RR is the respiration rate of the product expressed in mg CO2 kg−1 h−1. Then 180 represent glucose in g if this sugar is lost per 264 g of CO2 produced as a result of respiration rate (Saltveit, 2014). 2.2.3. Fruit flesh firmness Fruit flesh firmness was measured at the marked area of the mango fruit corresponding to the non-destructive measurements. The measurements were done using a SMS-P/4 cylinder on the texture analyser (TA-XT Plus, Stable Micro Systems, Surrey, UK) to penetrate the peeled tissue. The speed of penetration and depth of penetration was set at 200 mm min−1 and 8 mm, respectively. The maximum force (N) was analysed as mean from the two measurements. Six replicates were used for each treatment.

2. Material and methods 2.1. Plant material and storage conditions Mature green 'Shelly' mango fruit were obtained from Westfalia Marketing (Pty) Ltd, Hoedspruit, Limpopo, South Africa. The fruit were produced at Bavaria Fruit Estate, Hoedspruit, Limpopo Province, South Africa (latitude 24°22′45.5′'S, longitude 30°52′56.1′'E). Sound mango fruit were washed and subjected to standard hot water treatment (50 °C for 2 min) for postharvest disease control. Thereafter, mango fruits were cooled and waxed with Endura wax (Endura-fresh®, John Bean Technologies, Foodtech, Brackenfell, South Africa) adopted by the South African mango fruit industry. According to fruit size, 7–8 fruits were packed in well ventilated, corrugated card board cartons (25 × 40 x 10 cm) and air freighted to Berlin, Germany at 13 °C. Fruits were delivered at Department of Horticultural Engineering, Leibniz institute for Agricultural Engineering and Bioeconomy (ATB) in Potsdam, Germany 5 days after harvest. On arrival, fruits were further maintained at 13 °C and 85–90% relative humidity (RH) in walk-in cold room. The room captured 4 stainless steel chambers (190 L) connected to gas control system (Frigotec, Landsberg, Germany). Fruits were stored at O2 levels of 21, 10, 5, 1%, with CO2 set at 1% - all balanced to 100% with N2 and monitored at equidistant intervals. The N2 was

2.3. Analyses of pigments and colour 2.3.1. Non-destructive pigment analysis Fruits were measured non-destructively in the equatorial region of the fruit cheeks and the cut fruit pulp, with two measurements per fruit using a digital chromameter (CM-2600d, Konica Minolta Sensing Inc., Tokyo, Japan) and analysed on the basis of CIE colour system L*, a*, b*, Chroma (C) and hue angle (hº). For calibration, white and black tile was used(Caleb et al., 2016). Additionally, yellowness index (Iy) was calculated using the following equation (Nagle et al., 2016).

Iy =

1.2746L *−1.0574b * x 100 a*

(2)

The hand-held photodiode array spectrophotometer (Pigment Analyzer 1101, CP, Germany) was applied for measuring remittance spectra of the fruit at the same location of colour analysis. The light source is represented by five light emitting diodes in a light cup to measure relative changes in chlorophyll content, expressed as normalized differential vegetation index, NDVI = (I780 − I660)/(I780 + I660) 175

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40 ml of 10% sodium sulphate were added for phase separation. The supernatant was filtered through a 0.2 μm syringe and injected to the HPLC system (Prominence, Shimadzu, Germany) equipped with a PDA detector. Using XBridge C18 (4.6 x 250 mm) column with a spherical particle size of 3.5 μm (Cluzeau, France). Standards used were chlorophyll (a, b), pheophytin, carotenoids (Neoxanthin, Violaxanthin and βcarotene) (Roth Karlsruhe, Germany). In each case 10 μl of the individual external standards were injected and the areas values. Contents were then calculated from the calibration with standards expressed as μg g FW−1. Pigments were identified by comparing retention time (ret.time) and absorption spectra of the peaks for carotenoids, and fluorescence for chlorophyll.

measuring the absorption of chlorophyll pool at its red absorption peak. The NDVI resulted in normalized values ranging between −1 (low chlorophyll) and +1 (high chlorophyll). White calibration was performed using 80% Spectralon (Labsphere Ltd., USA) (Zude, 2003; Zude et al., 2007). Additionally, spectral data of mango samples were collected in diffuse reflectance mode using UV/VIS/NIR spectrophotometer (Lambda 950, PerkinElmer, USA) equipped with integrating sphere for measuring the diffuse reflectance of intact mango. System was operated on firm software (PerkinElmer UV WinLab Explorer). The spectra were recorded in 2 nm intervals capturing spectral range of 350–800 nm, similar to handheld readings, addressing the absorption of green and red pigments. Fruits were marked and placed in the equatorial region on the aperture of integrating sphere, which was tightly closed with black cover to prevent entrance of external light. For calibration, Spectralon (Labsphere Ltd., North Sutton, USA) was used as the 100% white reference for calculating the diffuse reflectance of the fruit as percentage of the reflection of the white reference (Seifert et al., 2014; Pflanz and Zude, 2008). As data pretreatment, mean centering was applied subtracting the mean of the entire spectrum of each reflectance intensity measured from the fruit spectrum to reduce the impact of varying scattering properties of the fruit. The grouping of the spectral data was done by principal component analysis (PCA) and scores were used to build calibration models for classes using the Soft Independent Modelingof Class Analogy (SIMCA) routine. The input variables captured the entire wavelength range. Spectral measurements were taken from two opposite points of the sample (n = 6). Fruit spectra were acquired at initial stage and weekly until 21d of storage at 13 °C under O2 storage conditions (21, 10, 5 and 1%) and again after keeping in shelf life for 7 days at 18 °C. Six replicates were used for each treatment. Additionally to the chlorophyll related NDVI, the following pigment indices were used to address red pigment contents from spectral measurements. The plant senescence reflectance index (PSRI) was calculated at the intensities (I) given according to (Merzlyak et al., 1999) as

PSRI = I 678 −

I 500 I 750

2.4. Chemical analysis Soluble solids content (SSC) of homogenous juice was obtained from three 2 × 2 × 2 cm cubes of pulp, from three separate parts of the fruit at different positions of the individual fruit. It was measured using a hand refractometer (DR301-95, Krüss Optronic, Hamburg, Germany) and expressed as %. Individual sugars were measured using a previously reported method (Caleb et al., 2016). Fruit sample (3 g) were transferred into Erlenmayer flask and diluted with Milli-Q water diluted 1:10 (g/v) and shaken for 30 min to have clear sample mixture. Subsequently, 2 mL of Carrez I solution (zinc sulfate, 300 g L−1) and 2 mL of Carrez II (potassium hexacyanoferrate, 150 g L−1) was added consecutively. Then 100 mL Milli-Q water was added into the flask and the solution was filtered through a membrane filter of 0.2 − 0.45 porosity. Sugar content (glucose, fructose and sucrose) were determined by HPLC method using a DIONEX Ultimate 3000 liquid chromatograph fitted with WPS-3000TSL Analytical auto-sampler (Thermo Fisher Scientific GmbH, Dreieich, Germany). The system is equipped with a refractive index detector SHODEX RI-101 (Showa Denko Europe GmbH, Munich, Germany). For separation, Eurokat H column (300 × 8 mm and 10 μm diameter) (KNAUER Wissenschaftliche Geräte GmbH, Berlin, Germany), with 0.01 M sulfuric acid as the mobile phase was used. The injected volume was 10 μL and at a flow rate of 0.8 mL min−1 operated at 35 °C A refractive index detector (RI71, Shodex, Techlab, Germany) was used with calibration of standards of glucose, fructose, and sucrose (Merck, Germany). Samples were identified by comparing retention time obtained and the retention time of the calibration standards and results were quantitatively expressed in g L−1 of fresh mango juice.

(3)

The total carotenoid to chlorophyll ratio was carried out with structure insensitive pigment index (SIPI), according to (Penuelas et al., 1995) as

SIPI =

I 800 − I 445 I 800 − I 680

(4) 2.5. Sensory evaluation, including ripening stages

2.3.2. Chromatographic pigment analysis Pigments were extracted and analysed of six fruits per treatment. Fruits were cut from equatorial positions previously marked for nondestructive pigments analysis. The 5 g of fresh mango pulp samples from two positions were merged for the analysis. Samples were directly homogenized with 0.2 g calcium carbonate to neutralise the fruit acid and 15 ml methanol using T25 Ultra-Turrax (IKA, Germany) for 2 min. The homogenate was filtered adding methanol until retained solid became colourless. The extraction was mixed with 50 ml of hexaneacetone (1:1, v/v) containing 0.1% of BHT. After a vigorous stirring

On each sampling day prior to further analysis, an organoleptic evaluation of fruits in terms of colour, texture, taste, odour and acceptance was done by six expert panelists who are regular consumers and familiar with mango fruit quality attributes (Table 1). The ripening stages were adapted from other cultivars of similar features. The fruit peel colour change was evaluated according to industry hedonic scale guidelines throughout storage. The ripening stages were classified into six different categories based on colour change from 0 to 100% yellow colour development on peel surface (Table 2). After harvest the fruit

Table 1 Sensory evaluation of 'Shelly' mango. Descriptors

Colour Odour Acceptance Texture Taste

Scores and description 1

2

3

4

5

< 10% yellow Dislike extremely (off odour) Unacceptable Extremely soft, no resistance to finger pressure Unacceptable

20 -30% yellow Dislike moderately Slightly unacceptable Moderately soft

50 -60% yellow Like/Dislike Moderately Minor signs of softness and loss of turgidity Moderately

70 - 90% yellow Like slightly Slightly acceptable Slightly firm, loss of turgidity, slight yield to finger pressure Slightly acceptable

100% yellow Like extremely (Fresh fruit odour) Acceptable Very firm and turgid, delayed yield to finger pressure Acceptable

Slightly unacceptable

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Table 2 Visual appearance used for classifying the fruit into ripeness stages of 'Shelly' mango. Ripening stages 1 (0–10%)

2 (10–30%)

3 (30–50%)

4 (50–70%)

5 (70–90%)

6 (90–100%)

peel colour surface was green with few red blushes, therefore we considered skin colour change from green to yellow. The sensory evaluation of mangoes was performed with six fruits from each treatment.

were used for each treatment. The experiment was repeated three times.

2.6. Measurement of volatile compounds (VOC)

3. Results and discussion

VOCs were sampled from six fruits stored for 5 d in air at 13 °C after harvest and from three fruits stored for 21 d at 13 °C in different O2 storage conditions (1, 5, 10 and 21%). After removal from storage chamber, each fruit was cut and three 2 × 2 × 2 cm cubes were cut from pulp from three separate parts of the fruit to obtain a homogenous VOC profile of whole fruit. After pressing the pulp cubes 1 mL of juice was transferred into 20 mL SPME vial (ND20, Carl Roth GmbH + Co.KG, Germany). After approx. 1.5 h of equilibration at 20 °C each vial was automatically transferred to an incubator of AOC 6000 PA L System autosampler (Shimadzu, Switzerland). Each vial was incubated for 15 min at 40 °C before extraction. VOCs from the headspace of the vial were automatically extracted by 50/30 μm divinylbenzene/ carboxen/ polydimethylsiloxane stableFlex/SS SPME fiber (Supelco, Bellefonte, PA, USA) for 10 min at 40 °C. VOCs extracted by SPME were desorbed at 250 °C in an inlet of a GCMS-QP2010 SE gas chromatograph – mass spectrometer (GC–MS; Shimadzu Europa GmbH, Duisburg, Germany) operating in splitless mode and equipped with a SPME liner (0.75 mm × 5.0 × 95 for Shimadzu GCs; Restek, Bellefonte, PA, USA). VOCs were separated on a DB-WAX (Agilent Technologies, Palo Alto, CA, USA) column (30 m × 0.25 mm × 0.25 μm). The initial GC temperature was 35 °C (hold 5 min) then the temperature increased to 250 °C at 5 °C min−1 (hold 5 min). Helium with a flow rate of 0.8 mL min−1 was used as a carrier gas. MS operated in electron impact mode at 70 eV and recorded mass spectrum in full scan mode (35–250 m/z). A two-step identification procedure has been performed. Firstly, mass spectra of VOCs were compared with the mass spectra from NIST v2.0f library (NIST, 2008). Then, retention index was calculated for each VOC according to van Den Dool and Kratz (1963) and compared with van Den Dool and Kratz RIs (polar column; temperature ramp) for DB-WAX or similar stationary phases using online NIST database (http://webbook.nist.gov/ chemistry/). C7-C30 saturated alkane standard (1000 μg mL−1; Supelco) were used for determination of RIs. Peak area of each VOC was integrated based on the quantifier and qualifier ions characteristic for its mass spectrum (Table 6) using MSD ChemStation E.02.01.1177 (Agilent Technologies, Palo Alto, CA, USA).

3.1. Changes in the gas composition during storage The reduction of O2 in the chambers took approximately 1 d for 21, 10 and 5% and 2 d for 1% O2 storage conditions. Slight fluctuations were observed however the O2 remained unchanged throughout storage after reaching equilibrium (Fig. 1a). The consistent flushing of N2 in controlled storage is vital to stabilize the desired gas composition throughout storage, reducing the O2 concentration in storage chambers. Meanwhile the CO2 concentration was initially enhanced, it stabilized with O2 reduction. Resulting with rapid decrease of CO2 in chambers containing high O2 concentration in approximately 1 d of mango storage and 6 d in reduced O2 concentration of 1%. The CO2 concentration stabilized, but increased slowly with fruit ripening and significantly in 21% O2 storage condition (Fig.1b).

2.7. Statistical design and analysis Statistical analyses were performed using free available chemometric statistical software package ‘R and RStudio’ version 1.1.442. Data was analysed by one way analysis of variance (ANOVA) at 95% confidence interval to evaluate the effect of O2 storage conditions on the quality attributes. The significance among mean treatment values were determined by least significant difference (LSD) and Tukey Post hoc tests at P < 0.05 level. Six replicates were used for each treatment. To determine the correlation of pigment indexes and pigment content, Pearson correlation coefficient was calculated and six replicates (n = 6)

Fig. 1. Fluctuation of gas composition considering O2 (a) and CO2 (b) during storage of ‘Shelly’ mango for 21 d at 13 °C in adjusted percentage of O2: 21, 10, 5, and 1%. 177

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Fig. 2. Respiration rate of ‘Shelly’ mango stored in adjusted O2 condition (21, 10, 5 and 1%) for 21 d at 13 °C.

3.2. Respiration Storage under the CA with different concentration of O2 affected (p < 0.05) the respiration rate of 'Shelly' mango fruit (Fig. 2). Similar results were presented in CA storage with 1%, 5% and 10% O2 for storage of ‘Palmer’ mango fruit (Teixeira et al., 2011). The fruit stored under low O2 concentrations of 1% and 5% presented the lowest respiration rates of 45.3 and 47.3 mg CO2 kg−1. h−1, respectively, throughout storage period from initial respiration rate of 24 mg CO2 kg−1. h−1. A gradual increase in respiration was found with storage period under all storage conditions. Climacteric fruits such as mango are characterised by an increase in respiration rate during ripening process. However, although there was an increase with storage time, low O2 storage conditions limited respiration rate (Fig. 2). Similar results considering gas composition, but also low temperature in treeripe ‘Irwin’ mango fruit (Nakamura et al., 2004).

Fig. 3. Mass loss and the values on top of the bar represent the percentage of substrate loss contributing to mass loss (a) and fruit flesh firmness (b) of ‘Shelly’ mango stored in different O2 conditions (21, 10, 5 and 1%) for 21 d at 13 °C.

3.4. Pigments and colour 3.4.1. Analysis of reflectance spectra During ripening, the average reflectance spectra of the fruits stored in different O2 conditions had similar pattern compared to measurements carried out before storage (initial spectra). However, only marginal pigment variation was observed at 450 nm, which is related to the presence of carotenoids pigment. A similar trend was presented for various mango cultivars such as 'Cogshall', 'Kent', 'Caro', 'Sensation', 'Tommy Atkins', 'Nam Doc Mai', 'Irwin' and 'Heidi' (Nordey et al., 2014). However, as the fruits had red blushes, the related varying anthocyanins, absorbing with a broad peak maximum at 550 nm, can be expected to perturbate the correlation of spectral data and carotenoids due to coinciding absorption. Results suggest that there is no unique relationship between different O2 storage conditions (21, 10, 5 and 1%) and red pigments (Fig. 4). In contrast, fruits at 1% O2 could be visually (data not shown) separated from the remaining treatments. It is assumed that the scattering properties of the tissue may change in hypoxic conditions, which was not recognized by the reflectance readings. The increase in reflectance spectra at 680 nm can be linked to chlorophyll degradation with ripening of the fruits compared to initial spectra (Fig. 4). Hereby, the maximum absorbance of the chlorophyll pool in vivo is at 680 nm (Seifert et al., 2014). Interestingly, at 680 nm there is slight variation observed among the different O2 storage conditions, fruits stored in 21% O2 resulted with highest chlorophyll degradation (Fig. 4). This variation provides basis for determining the fruit ripening stages (Seifert et al., 2014; Ullah et al., 2016,). The scores of the principle component analysis of spectroscopy data point to pigment shift with fruit ripening, but irrespective of different O2 storage conditions. The clustering could be observed according to weeks of storage, separating unripe and ripe fruits, while no clustering appeared according to the treatment. However, overall statistical analysis of fruit

3.3. Fruit mass loss and flesh firmness Fruit mass loss increased with storage time, data not shown. However, it was clear that low O2 storage conditions of 1% reduced respiration rate, resulting in reduced mass loss compared to 21% showing highest mass loss of 3% after 21d of storage (Fig. 3a). The observed increase in substrate loss could be due to high respiration rate under 21% O2 storage, resulting in loss of food reserves in the tissue (Saltveit, 2014). Mass loss was found to increase as the storage period was prolonged, which is assumedly due to heat generated by respiration and transpiration. Accumulation of respiratory heat during respiration, increases the water vapour partial pressure within the fruit (Maguire et al., 2000). An increased fruit temperature, the vapour pressure deficit (VPD) between the fruit and the storage atmosphere is enhanced (Whitelock et al., 1994) and this results in increased moisture loss at 21% O2. In this study, as expected, fruit firmness decreased drastically during storage with ripening. There was a significant decline in fruit firmness in all storage conditions from 140 N to 18 N (1% O2) and 14 N (5% O2) at 21d (Fig. 3b). Nevertheless, the fruits stored in 1% O2 storage conditions presented consistent maximum retention of tissue strength during storage. The gradual textural softening is due to a series of increased activity of cell wall degrading enzymes such as polygalacturonase, pectin methylesterase, β-galactosidase, and β -glucanase (Hossain et al., 2014). Furthermore, the assumed decrease of cell turgor pressure due to moisture loss accelerated the process. A similar reduction in fruit firmness was reported in 'Shelly' mango fruit stored for a period of 4–6 weeks at 10 °C and exposed to shelf-life conditions of 20 °C for a period of one week (Kumar et al., 2018).

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Table 4 Pearson correlation coefficients (r) and probability level (p) for the relationships between pigment indexes and the main pigment content in 'Shelly' mango. Pigment index Correlations

Violaxanthin Zeaxanthin Lutein Total carotenoids Chlorophyll a Chlorophyll b Total chlorophyll

PSRI

SIPI

NDVI

r

p

r

p

r

p

0.59 0.70 0.67 0.69 −0.70 −0.54 −0.70

0.013 0.002 0.004 0.002 0.002 0.025 0.002

0.55 0.66 0.57 0.64 −0.64 −0.45 −0.67

0.022 0.004 0.017 0.006 0.006 0.069 0.003

−0.73 −0.71 −0.75 −0.75 0.70 0.63 0.74

0.001 0.001 0.001 0.001 0.002 0.007 0.001

PSRI = Plant senescence reflectance index, SIPI = Structure insensitive pigment index, NDVI = Normalized differential vegetation index. Fig. 4. Mean diffuse reflectance spectra of ‘Shelly’ mango peel measured nondestructively.

chlorophyll content that decreases with fruit ripening (Table 4) as shown earlier for apple (Zude, 2003). The assessment of pigment contents in fruit using spectral reflectance measurements on the peel is reported to assume that the optical pigment features remain the same. However, it is cultivar dependent and surface reflectance is affected by various factors. Nordey et al. (2014) even reported accuracy of R2 > 0.91, RMSE < 5.75 μg g FW−1 for assessing pigment content in various mango fruits using reflectance spectroscopy.

Table 3 Classification of fruit in the calibration model and validation results obtained using SIMCA. Set

Week Week Week Week Week

n

1 2 3 4 5

24 24 24 24 24

Calibration

Validation

Correct sample

Misidentified sample

None

Correct sample

Misidentified sample

None

100 91.7 100 100 100

0 8.3 0 0 0

0 0 0 0 0

91.7 83.3 91.7 83.3 91.7

0 16.7 0 0 0

8.3 8.3 8.3 16.7 8.3

3.4.3. Fruit pulp colour Storage time and gas composition had significant effect on colour parameters of 'Shelly' mango fruit. The increase of the intensity of the yellow orange colour of the fruit pulp was accompanied by an increase in the values of a* and b* and a reduction in L* and hº colour values during storage (Table 5). Similar results for a*, b*and L* have been reported in storage of 'Manila' and 'Ataulfo' mangoes (Ornelas-Paz et al., 2008). There was significant difference observed among the treatments, and fruits stored under 1% O2 resulted with least yellow index of 103.7 ± 1.2. This shows that low O2 had an impact on delaying chlorophyll degradation. However, this assumption was not proved neither by the chromatographic nor spectral analyses. Consequently, we assume that changes in the colour appeared due to changes in the scattering features affected by the storage conditions. Further in depth study separating absorption and scattering coefficients would be necessary here. The low values of h° in pulp indicate a deep orange-yellow colour as observed in fruit stored in 21% O2, while high a* values have been related to a high β-carotene content, but could also point to high chlorophyll content (Ornelas-Paz et al., 2007). Resulting, the colour analysis appears less specific compared to HPLC and spectral analyses.

spectra and chromatographic data showed encouraging results for nondestructive analysis of pigments considering the visible range of 350–800 nm in 'Shelly' mango as shown below and, consistently, SIMCA results yielded high capacity for classifying fruit ripening stages (Table 3). This was partly expected due to the development of yellow colour in fruit peel and pulp was induced by the biosynthesis of carotenoids and, mainly, degradation of chlorophyll during fruit ripening in storage (Nordey et al., 2014). 3.4.2. Correlation between pigment indices and pigment content The reflectance spectra of mangoes were used to calculate plant senescence reflectance index (PSRI) and structure insensitive pigment index (SIPI) addressing the carotenoids and anthocyanins. Additionally, the normalized differential vegetation index (NDVI) should appear linked with the chlorophyll pool. The chlorophyll content in the pulp varied from 0.02 to 1.46 μg g FW−1 according to fluorescence signal of chlorophyll a, and from 0.03 to 2.14 μg g FW-1 for chlorophyll b. Meanwhile carotenoids varied from 0.00 to 10.57 μg g FW−1 for absorption-recognized neoxanthin, from 0.60 to 8.01 μg g FW−1 for violaxanthin, from 0.00 to 17.46 μg g FW−1 for zeaxanthin, from 0.00 to 12.46 μg g FW−1 for lutein, and from 0.03 to 2.14 μg g FW−1 for total carotenoids. Coefficient of determination of PSRI and SIPI and carotenoids was R2 = 0.71 at maximum. The positive correlation of PSRI and carotenoids has previous been reported in apple fruit, due to significant increase in carotenoids in the peel of the ripening fruit (Merzlyak et al., 1999). It can be assumed that the negative correlation of R2 = -0.72 between PSRI and chlorophyll content is an indirect indicator of chlorophyll degradation and accumulation of carotenoids during mango ripening. The relationship between PSRI and pigment contents makes it possible to analyse fruit ripening stages, according to changes in the spectral reflectance near 500 nm and 680 nm. Meanwhile, NDVI was related to chlorophyll a, b and total chlorophyll with R2 > 0.70, R2 > 0.63, R2 > 0.74, respectively. In conclusion, these pigment indices can be used to non-destructively predict the mango

3.5. Sugar analysis The SSC of 'Shelly' mango increased from 10.67 before storage to 15.90, 16.25, 14.87 and 15.18 in 21, 10, 5 and 1% O2, respectively (Fig. 5a). Similar results have been reported in 'Shelly' mango by Kumar and co-workers (Kumar et al., 2018) and the increase in SSC content indicated ongoing ripening process. Bender et al. (2000) reported starch and sugar breakdown in 'Haden' and 'Tommy Atkins' mango stored for 21 d in 2–5 % O2. This indicate that sweet taste in mango fruit increased with ripening as a result of gluconeogenesis, accumulation of sugars (sucrose, glucose and fructose), hydrolysis of polysaccharides particularly starch and reduction in organic acids (Cortés et al., 2016). Highest SSC was observed in fruits stored in 21% and 10% O2 conditions, this shows that at low O2 concentrations the breakdown of starch molecules into glucose, through the action of amylases and/or glucose-1-phosphate, by the enzyme phosphorylase, could have been reduced and resulted with lowest SSC in 1% and 5% O2 concentrations (Teixeira et al., 2011). Additionally, the major sugars were identified as fructose, glucose, and sucrose with initial sugar contents of fructose, 3.05 ± 0.39, glucose 1.18 ± 0.13, and sucrose 3.19 ± 1.23 g/100 g 179

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Table 5 Fruit pulp colour parameters (L*, a*, b*, C*, hº and yellow index) in 'Shelly' stored in different O2 storage conditions (%) of 21, 10, 5 and 1 for 21 d. Colour parameters

Initial

O2 gas composition (%) 21

Lightness (L*) Redness (a*) Yellowness (b*) Chroma (C*) Hue (hº) Yellow index

a

77.6 ± 1.0 8.0 ± 1.8b 55.8 ± 1.9b 67.2 ± 1.5a 78.7 ± 0.6a 93.1 ± 3.7c

10 b

5 ab

74.7 ± 0.9 18.7 ± 1.3a 73.2 ± 7.6a 75.6 ± 7.5a 75.7 ± 1.3b 140.0 ± 14.6a

75.6 ± 0.9 16.1 ± 1.9a 68.8 ± 0.8a 70.7 ± 0.5a 76.9 ± 1.7ab 130.2 ± 1.7ab

1 b

74.5 ± 1.3 15.8 ± 1.2a 63.7 ± 4.4ab 65.7 ± 4.3a 76.0 ± 1.5ab 122.1 ± 7.1b

75.3 ± 1.8ab 16.6 ± 2.2a 67.7 ± 5.6a 69.7 ± 5.9a 76.3 ± 1.1ab 103.7 ± 1.2c

3.7. Volatile compounds

FW (Fig. 5b). Individual sugars increased with storage time and sucrose was the predominant sugar and fructose the major reducing sugar in all treatments with no significant difference between them. Similar results were reported in 'Keitt' (Tian et al., 2010) and in 'Tainong No1′, 'Irwin', 'Jinwang' and 'Keitt' mango (Liu et al., 2013). The changes in sucrose content during the storage period were found consistent with other studies in the literature. Previous studies showed that sucrose is the predominant sugar that accumulates in the fruits during storage and ripening, contributing over 60% of the total soluble sugars in ‘Haden’ mango fruit (Castrillo et al., 1992). The glucose concentration increased slightly with storage time. However, it contributed a low amount of 16% to the initial total sugars compared to sucrose and fructose contributing to the biosynthesis of sucrose and fructose during the ripening process as the carbohydrates hydrolysis (Bello-Pérez et al., 2007). On the other hand, fructose increased gradually during fruit storage. According to Moore (2003), the fructose reducing power protects the carotenoids from oxidation, thus in return preserving the quality of the fruit colour and antioxidant activity of the carotenoids.

A total of 29 O2 restricted metabolites were found in this study. O2 storage conditions significantly affected production of fermentative VOCs (p > 0.05). Different O2 concentrations in storage chambers influenced individual VOCs differently (Table 4). The VOCs found in 'Shelly' mango fruit included various classes such as (a) aldehydes, (b) alcohols, (c) esters, (d) ketones, (e) dioxolane, (f) dialkyl ethers, (g) alkanes and two unknowns. At the end of storage, the majority of VOCs detected in the restricted O2 samples were esters, particularly ethyl acetate (23.41 a.u.), ethyl butanoate (8.84 a.u.) and ethyl 2-methyl-2butenoate (0.19 a.u.). In contrast, under moderate O2 storage conditions, these compounds were relatively unchanged (Table 6). The most emitted ester under restricted O2 was ‘ethyl acetate’ and is reported to have a contribution to undesirable flavour due to its solvent-like aroma. Esters are formed by the action of alcohol acyltransferase (AAT) enzymes and fermentative metabolism which can be enhanced in fruit via various stress factors such as intrinsic (ripening, senescence), biotic (microbial growth) factors and extrinsic (temperature, hypoxic conditions – in this case reduction of O2 concentration in CA storage (White et al., 2016; Caleb et al., 2013). Interestingly, ethyl butanoate was reported to significantly contribute to the fruity attributes in mango fruit (Pino et al., 2005). Similarly, in 'Delta R2E2′ mangoes the concentrations of ethyl acetate and ethyl butanoate was significantly (P ≤ 0.05) higher in the pulp of ripe fruit CA-stored for 38 d in 1.5% O2 and 6% of CO2 (Lalel and Singh, 2006). The concentrations of alcohols detected were significantly higher in fruit stored in 1% O2 storage conditions and decreased as the O2 concentration in the storage chamber was increased (Table 6). The most abundant alcohol detected in 'Shelly' mango fruit was ethanol (58.10 a.u.), 1-butanol (3.08 a.u.), [S-(R*,R*)]-2,3-butanediol, 2,3-butanediol acetol (0.99 a.u.), Propylene glycol (0.95 a.u.) and 3-methyl-1-butanol (0.68 a.u.). Thus, this observation suggests that reduction of O2 storage concentration to 1% had the negative impact on the aroma profile of 'Shelly' mango and it should be avoided. This may be attributed to fermentative metabolism in the fruit due to anaerobic conditions, which led to an ‘off-flavour’. White et al. (2016) reported that under anaerobic conditions acetaldehyde and ethanol are basically controlled by pyruvate decarboxylase and alcohol dehydrogenase (ADH). The ADH is an oxidoreductase which is responsible for converting acetaldehyde to ethanol. Previously, ethanol has been reported in fruit and vegetable (apples, strawberries, broccoli and wild rockets) stored under restricted O2 conditions and is currently used as a biomarker of restricted O2 conditions during storage (Luca et al., 2016). Therefore, optimal O2 storage concentrations for 'Shelly' mango fruit are > 5% O2, to avoid accumulation of fermentative metabolites.

3.6. Sensory aspects Fig. 6 illustrates the sensory evaluation of 'Shelly' mango. The panelist’s perceived fruits stored in 21 and 10% O2 storage conditions to be more acceptable (higher overall acceptance), based on uniform attractive colour and taste. Interestingly, the fruits stored in 21% O2 storage conditions were not preferred in terms of texture (firmness) at the score of 2. In terms of colour and acceptance there was no differences noted between fruits stored in 21, 10 and 5% O2 storage conditions. This showed that the reduction in O2 concentration to 1% compromised the sensory quality of mangoes within 21d of storage, resulting with slight development of ‘off-flavour’ in fruit taste, although the fruits were firmer compared to other storage conditions. Irrespective of different O2 storage conditions the mango fruits ripened. The degree of ripeness plays a major role in the assessment of sensory and acceptability. Therefore, fruits are accepted according to physical appearance, such as yellow colour development. In this study, 100% of fruits before storage were classified in ripening stage 1 showing 0% uniform yellow colour. Since the fruits successfully ripened, there were no fruits classified in RS 2 and 3 at 21 d (Fig. 7). About 80% of fruits stored in 21 and 10% O2 storage condition showed to have fully ripen with 90–100% yellow colour on fruit surface. Fruits stored in 5% O2 storage condition showed uneven ripening. However, low O2 storage conditions delayed ripening and 70% of fruits stored at 1% O2 were classified in ripening stage 5, representing 'Shelly' mango with peel surface area of 70–90% yellow colour (Table 2). Lalel et al. (2005) reported significant (P ≤ 0.05) delay and reduction in skin colour development in 'Delta R2E2′ mangoes stored in CA storage conditions of 1.5, 2 or 3% O2 and 6% or 8% CO2 compared to control.

4. Conclusion It is evident from this investigation that 'Shelly' mango fruit can be 180

181

9.63 9.64 11.24 11.52 13.20 13.31 13.85 15.33 15.47 15.74 19.82 21.86 22.54 23.46 23.81 27.33 30.55

3.42 3.60 4.72 5.11 5.35 5.58 5.59 5.75 7.46 7.81 8.49 8.62

1100 1100 1151 1160 1213 1216 1233 1280 1285 1293 1439 1519 1549 1588 1603 1752 1900

< 900 < 900 938 953 963 972 972 978 1035 1045 1066 1069

RI

– 1100 1116-1166 1158 1195-1255 1196-1245 1223 1250-1332 – 1275-1317 – 1484-1522 1539-1580 – 1600-1605 1761

839-904 863-908 900-955 939-976 957-971 952-996 978 – 1000-1073 – 1049-1100 1049-1105

LRI

– 1120-21-4 71-36-3 10544-63-5 123-51-3 109-21-7 55514-48-2 513-86-0 – 116-09-6 19780-35-9 5405-41-4 513-85-9 19132-06-0 57-55-6 629-82-3 629-92-5

123-72-8 141-78-6 64-17-5 105-37-3 97-62-1 109-60-4 96-22-0 3299-32-9 105-54-4 4358-59-2 108-64-5 123-86-4

CAS

Unknown1 Undecane 1-Butanol Ethyl ester 2-butenoic acid 3-Methyl-1-butanol Butyl butanoate Ethyl 2-methyl-2-butenoate 3-Hydroxy-2-butanone Unknown2 Acetol Ethyl 2,3-epoxybutyrate Ethyl 3-hydroxybutyrate 2,3-Butanediol [S-(R*,R*)]-2,3-Butanediol Propylene glycol Octyl ether Nonadecane

Butanal Ethyl acetate Ethanol Ethyl propanoate Ethyl isobutyrate Propyl acetate 3-Pentanone 2,4,5-Trimethyl-1,3-dioxolane Ethyl butanoate (Z)-Methyl ester 2-butenoic acid Ethyl isovalerate Butyl acetate

VOC

68, 43, 41, 41, 43, 43, 55, 43, 69, 43, 45, 60, 45, 45, 45 43, 43,

41, 43, 43, 43, 71, 43, 57, 55, 43, 41, 57, 56,

102 88

114 71 56 99 70 89 113

101 88 100 88 73

72 70 46 102 116

57, 71 57, 71

86, 57, 43, 69, 55, 71, 83, 45 86 74 74, 71, 57 57

57, 61, 45, 57, 88, 61 86 73, 71, 69, 85, 61,

Ions used for quantification and qualification (m/z)

0.00b 0.00b 0.00b nd 0.00b nd 0.00b 0.62b nd 0.00c nd nd 0.00b 0.01b 0.00b 0.25b 0.00b

nd 0.11b 2.23b nd nd nd 0.05b nd 0.02b nd nd nd

Initial

30.79a 1.93a 3.08a 1.05 0.68a 0.53 0.19a 13.02a 0.34 0.99a 0.71 0.27a 1.99a 2.28a 0.95a 0.93a 0.05a

0.08 23.41a 58.10a 2.27 0.09 0.11 0.53a 0.41 8.84a 1.34 0.55 0.21

1

0.18b 0.00b 0.05b nd 0.04b nd 0.01b 2.39b nd 0.42b nd nd 0.44b 0.70b 0.20b 0.47ab 0.03ab

nd 0.30b 4.27b nd nd nd 0.64a nd 0.03b nd nd nd

5

0.00b 0.04b 0.01b nd 0.02b nd 0.00b 0.07b nd 0.10c nd nd 0.00b 0.00b 0.02b 0.04b 0.00b

nd 0.03b 2.43b nd nd nd 0.21b nd 0.00b nd nd nd

10

O2 Storage conditions (%)

0.00b 0.00b 0.00b nd 0.01b nd 0.00b 0.03b nd 0.11c nd nd 0.00b 0.00b 0.00b 0.05b 0.00b

nd 0.01b 1.92b nd nd nd 0.16b nd 0.00b nd nd nd

21

< 0.001 < 0.001 < 0.001 ns < 0.001 ns < 0.001 < 0.001 ns < 0.001 ns ns < 0.001 < 0.001 < 0.001 0.012 0.007

ns < 0.001 < 0.001 ns ns ns < 0.001 ns 0.003 ns ns ns

P

– Ethereal, pineapple Alcoholic – Citrus, strawberry Celery – – Fruit Balsam, spicy Apple Banana, fruity, sweet, green – – fermented – Oily, whiskey – Raspberry, caramel, fruity – – – – Grape, sweet – – – – –

Aroma descriptor*

RT = Retention time, RI = Retention index, LRI = Linear retention index, CAS = CAS number, VOC = Volatile organic compounds. The means followed by common letters in each column are not significantly different at (P < 0.05).*SAFC-Flavors and Fragrances (2008),; Zhang et al. (2017), Alvarez et al.2011, Rice and Koziel (2015).

13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29

1 2 3 4 5 6 7 8 9 10 11 12

RT

Table 6 Selected volatile compounds released from 'Shelly' mango stored under different O2 conditions (21, 10, 5 and 1% O2) for 21 d and results from ANOVA are shown in the table.

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Fig. 7. Ripening stages (RS) of ‘Shelly’ mango stored in different O2 conditions (21, 10, 5 and 1%) for 21 d at 13 °C.

mango fruit. Future studies could use reflectance measurements for assessing pigment contents in the supply chain to monitor the quality of the mango fruit. Acknowledgements This work is based upon research supported by iPostTech project funded through German Federal Ministry of Food and Agriculture (BMEL) and the South African Research Chairs Initiative of the Department of Science and Technology and National Research Foundation of South Africa Grant No. 98352. The authors gratefully acknowledge Wegner Gabriele, Corinna Rolleczek, Kathrin Ilte and Giovanna Rehde (ATB, Potsdam, Germany) for technical assistance with laboratory analyses. We would also like to thank Westfalia fruit, South Africa for supply of fruits.

Fig. 5. Influence of O2 concentration on soluble solids content (SSC) (a) and individual sugars (b) of ‘Shelly’ mango stored for 21 d at 13 °C.

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stored in atmospheres containing between 5 to 10% O2. These conditions maintained quality attributes, delayed ripening process and reduced accumulation of O2 restricted volatile compounds. This shows the importance of maintaining an optimal low O2 limit in mango storage. Reduction of O2 concentration in storage chambers to 1% O2 resulted in detrimental effect on fruit aroma and taste, therefore it should be avoided. Flavour life of fruits stored in 1% O2 was shorter compared to postharvest shelf life. Different pigment indexes from spectral reflectance measurements were used to predict pigment content. However, accuracy may have been compromised as the fruits had red blushes on the peel, and low O2 had no significant effect on pigment content. In conclusion, the findings of this study provide useful information on optimal O2 conditions (5 and 10%) to retain overall fruit quality during CA storage and to extend the marketing chain of 'Shelly'

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