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. 2019 Aug 1;56(11):5074–5086. doi: 10.1007/s13197-019-03980-7

Evaluating the efficacy of chitosan and CMC incorporated with moringa leaf extracts on reducing peteca spot incidence on ‘Eureka’ lemon

Muriel Mbhoni Rikhotso 1, Lembe Samukelo Magwaza 1,2,✉, Samson Zeray Tesfay 1, Asanda Mditshwa 1,✉
PMCID: PMC6828921  PMID: 31741532

Abstract

Lemon (Citrus limon L.) is one of the most cultivated citrus fruit in South Africa. In citrus packhouses, fruit are coated with commercial synthetic waxes to enhance shelflife. However, the use of waxes has been linked to peteca spot (PS) incidence in lemons. This study evaluated the efficacy of chitosan (CH) and carboxymethyl cellulose (CMC) incorporated with moringa leaf extracts (M) on reducing peteca spot incidence on ‘Eureka’ lemon. A total of 500 ‘Eureka’ lemons were harvested from outside and inside canopy positions from a commercial orchard in KwaZulu-Natal, South Africa. Fruit were assigned to five coating treatments, namely; control, 1% M + CMC, 1% CMC, 1% CH and 1% M + CH. After coating, fruit were transferred into a cold room with delivery air temperature set at 3 °C for 12 weeks to induce the disorder. At each sampling week, peteca spot incidence, fruit physicochemical and phytochemical properties including color, mass, vitamin C, carotenoids, TSS, TA and phenolics were measured. The results showed that coating treatments and canopy position significantly affected PS incidence. Fruit coated with M + CMC, CMC, CH were less susceptible to PS development in both inside and outside canopy compared to the control and M + CH coated fruit. Coating treatments significantly affected phenolic and flavonoid concentration. Moreover, coating treatments significantly reduced mass loss, ascorbic acid loss and delayed color change of fruit. The results found in this study demonstrated the ability of either M + CMC, CMC, or CH as coating treatments for reducing PS in ‘Eureka’ lemon.

Keywords: Canopy position, Edible coatings, Physicochemical properties, Citrus, Peteca spot, Moringa

Introduction

Lemon (Citrus limon L.), belonging to the citrus family Rutaceae, is one of the most cultivated citrus cultivars in South Africa (Citrus Growers’ Association of South Africa 2018). Lemon plantings and exports have significantly increased in the past decade due to a global high demand of the fruit. This is largely attributed to the high nutritive and therapeutic characteristics of lemons (Iglesias et al. 2007). The 2018 estimated export production for lemon in South Africa is over 20 million tons (Citrus Growers’ Association of South Africa 2018). The most important lemon cultivar planted in South Africa is ‘Eureka’. During 2017 export season, the total area used for ‘Eureka’ plantings was 9097 ha which represents 83% of the total lemon planted in Eastern Cape and Limpopo provinces (Citrus Growers’ Association of South Africa 2018).

Lemons are characterized by high vitamin C content (0.53 g/kg in juice and 1.29 g/kg in peel) and other vitamins such as vitamin B, riboflavin and minerals, which are related to the prevention of various non-communicable illnesses such as cancer and cardiovascular disease (Silalahi 2002). After harvest, citrus fruit are prone to the development of rind physiological disorders which are caused by internal and external factors. For this reason, the fruit are usually coated with commercial synthetic waxes like thiabendazole or imazalil in order to reduce water loss and prolong shelflife (Palou et al. 2015).

Wax coating is applied on the surface of the fruit, which makes the probability of consuming the coating with the fruit high. This has raised concerns regarding health and environmental effects which are associated with chemical residues (Palou et al. 2015). Some waxes have been found to impair fruit quality and cause rind physiological disorders by restricting gas exchange through the peel, which causes anaerobic conditions in the internal atmosphere of the fruit (Arnon et al. 2015). Young and Biale (1968) alluded that the reason behind this occurrence could be attributed to the fact that the waxes restrict gaseous exchange resulting in increased carbon dioxide concentration which in turn increases the concentration of organic acids. The increase results in an overproduction of volatiles which are associated with anaerobic conditions. This causes calcium imbalances that may lead to the development of PS (Khalidy et al. 1969). For instance, polyethylene-based waxes are known for aggravating the incidence of PS in lemons (Wild 1991).

Peteca spot is a physiological disorder that causes a major loss in all citrus producing provinces in South Africa (Cronje 2015). The disorder occurs from time of harvest until cold storage and the symptoms can be seen 3–4 weeks after packing and sorting (Khalidy et al. 1969). A major problem relating to this disorder is that fruit are shipped to distant markets and the time of disorder development can coincide with the time the lemon reach the international market which can result in the rejection of the whole fruit consignments. This makes it important to find ways to reduce the PS incidence without impairing fruit quality and posing threat to human health. Consumer’s demands for healthy and high quality fruit has led to many countries changing their regulations and imposing limitations to the use of agrochemicals and synthetic waxes which has now led to a switch from synthetic waxes to edible coatings (Palou et al. 2015).

The use of edible coatings is increasingly becoming a core focus in postharvest handling, however, most of the edible coatings that have been evaluated on citrus fruit focused on hydroxypropyl methylcellulose, beeswax and shellac composites which require using powerful organic solvents like ammonia to dissolve resulting in restricted gas exchange (Sánchez-González et al. 2011). Among a wide variety of edible coatings, moringa, chitosan and CMC have been reported to dominate the food industry which is seen by the increasing published research for their use.

Moringa, incorporated with CMC was found to extend shelflife and maintain the quality of oranges (Adetunji et al. 2013). Tesfay and Magwaza (2017) evaluated the efficacy of CH and CMC incorporated with moringa on postharvest quality of avocados, their findings showed improved quality and extended shelf-life after 21 days of cold storage at 5.5 °C. Notably, the authors also found that CMC containing moringa extract is particularly able to suppress postharvest diseases and maintain quality of avocados. Extended shelflife was also reported in guava which was treated with chitosan-cassava starch coating before storage (de Aquino et al. 2015).

Chitosan and CMC coatings have previously been evaluated in various citrus fruit including ‘Navel’ oranges, ‘Star Ruby’ grapefruit as well as mandarins, and the coatings have been found to increase fruit firmness while sensory evaluations showed that fruit flavor was not impaired (Arnon et al. 2015). The success of moringa, CMC and CH to be used as edible coatings is mainly based on the fact that they are very affordable and preparation is quite simple. However, there is currently no research that has evaluated the potential of edible coatings as postharvest treatment of ‘Eureka’ which is the most important lemon cultivar. As a result, the citrus industry heavily relies on environmentally unfriendly synthetic chemicals for controlling various postharvest physiological disorders. Thus, it is important that non-chemical, innovative and novel postharvest treatments are developed for the citrus industry. The aim of this research study was therefore, to evaluate the efficacy of CH and CMC and their combinations with moringa leaf extracts on reducing the incidence of PS on ‘Eureka’ lemon.

Materials and methods

Fruit sampling

A total of 500 ‘Eureka’ lemons with an average mass ranging from (106.7 to 130.7 g) at harvest were harvested from Malowe commercial orchard located in uMzimkhulu, KwaZulu-Natal, South Africa (Latitude: 30°14′S, Longitude: 29°56′E). The size of the farm is 6 ha with 3300 trees. Five groups of five trees were strategically selected to represent the orchard, resulting in a total of 25 experimental trees. To evaluate the effect of light exposure on fruit response to coating treatments during storage, ten fruit from outside sun-exposed and ten from inside shaded positions of the canopy were harvested from each of the 25 trees, resulting in a total of 500 fruit. After harvesting, the fruit were transported to the University of KwaZulu-Natal research laboratory using a well-ventilated car.

Treatments and storage

Upon arrival to the laboratory, fruit were assigned to 5 coating treatments: T1: Control (untreated lemons); T2: Lemons treated with 1% M + CMC (moringa + carboxymethyl cellulose); T3: Lemons treated with 1% CMC (carboxymethyl cellulose); T4: Lemons treated with 1% CH (chitosan); T5: Lemons treated with 1% M + CH (moringa + chitosan). Fruit from two different canopy positions were treated with different coating treatments. The experiment was a two-factor factorial experiment arranged in a completely randomised design with canopy position as a first factor at two levels and postharvest coating treatments as a second factor at five levels.

The preparation of coating treatments was done according to a method described by Tesfay and Magwaza (2017). Briefly, 100 g of moringa leaf was extracted using 1 L of methanol/HCl 1% (v/v) for approximately 2 h with agitation at 4 C. A rotary evaporator was used to concentrate the extracts. Thereafter, 20 mL of distilled water was added and the crude extract was later subjected to sequential liquid–liquid extraction with hexane, chloroform and ethyl acetate. On the other hand, carboxymethyl cellulose was dissolved in warm double distilled water to obtain a final concentration of 1%. For chitosan, double distilled water and acetic acid were used to dissolve and acidify chitosan in order to obtain the required 1%. Fruit were immersed in assigned coating treatments for 1 min and left at room temperature for about 30 min for the coating to dry. The fruit were then packed and transferred to 3 °C to induce the development of PS (Undurraga et al. 2009). Each treatment consisted of a total of 50 fruit (5 replicates with 10 fruit per replicate). During storage, the treatments were arranged in a completely randomised design. Sampling was done for a period of 12 weeks at 3 weeks intervals and 10 fruit were selected per treatment for each sampling date.

Postharvest quality measurements

After coating treatments, the data for week 0 was collected and physico-chemical variables such as color, mass, total soluble solids (TSS) and total acidity (TA), ascorbic acid, and carbohydrates were measured. The same sampling procedure was repeated with fruit in cold storage. Fruit were destructively analyzed every 3 weeks for the period of 12 weeks and PS incidence was assessed and expressed as %. The PS index was calculated using Eq. 1 (0 = no peteca symptoms, 1 = moderate and 2 = severe) according to Cronje (2015).

PetecaIndex=∑Peteca0-2×No.offruitineachclassNumberoffruitinarep 1

On each sampling date, the rind was peeled using a peeler separating the flavedo and albedo and immediately stored at − 40 °C until further analysis. The frozen samples were freeze-dried using a VirTis Freeze dryer system (Model 6KBTES-55, SP industries, Warminster, PA, USA) for 7 days at (150–250 millitor) and − 40 °C. The dry samples were weighed and water content was calculated from freeze–dried samples and expressed as a percentage of dry mass, after which samples were ground into fine powder using a laboratory blender [OmniBlend (PTY) Ltd. Cape Town, South Africa].

Fruit mass and color index

The measurement of fruit mass was carried out using a calibrated weighing scale (RADWAG Wagi Electronic Inc., Poland). Fruit color was objectively quantified based on L*, a*, b* and h parameters measured using a portable colorimeter (Chroma Meter, Konica Minolta Sensing, INC., Japan). Color sampling was done from three random spots on the equatorial position of a fruit. Calibration of the instrument was done by scanning a 100% white reference brick with Y = 91.59, X = 0.3167 and y = 0.3315 prior fruit scanning. The parameters C* (chroma) and h* (hue angle) were calculated according to C* = (a*2 − b*2)1/2 and h* = arctan (a*/b*), respectively. The total color difference was expressed as a citrus color index (CCI) using Eq. 2 according to Vidal et al. (2013).

CCI=1000∗aL∗b 2

Determination of total carotenoids

The concentration of total carotenoid was determined and quantified using a method described by Corrêa et al. (2011) with slight modifications. A 150 mg ± 0.5 of the powdered sample used for the determination of total carotenoids was added into a test-tube, and 2 mL of 80% (v/v) acetone was added. The sample was centrifuged for 10 min using GenVac® (SP Scientific, Genevac LTD., Suffolk, UK). For maximum detection of carotenoids, six wavelengths (470, 646.8, 645, 505, 435, 663.2 nm) were used to measure the supernatant. The calculations for the concentrations of chlorophyll a (Ca), chlorophyll b (Cb), total carotenoids (Cx), β carotene and lycopene were done using Eqs. 3, 4, 5, 6 and 7:

Ca=12.25A663.2-2.79A646.8 3
Cb=21.5A646.8-5.10A663.2 4
Cx=(1000A470-1.82Ca-85.02Cb/198 5

where Ca = Chlorophyll a, Cb = Chlorophyll b, Cx = total carotenoids

βcarotene=0.216A663.2-1.22A645=0.304A505+0.452A453 6
Lycopene=-0.0458∗A663+0.204∗A645+0.372∗A505-0.0806∗A435 7

Determination of TSS and TA

Total soluble solids (TSS) and total acidity (TA) was determined using a hand squeezed juice from 10 fruit per treatment. TSS was measured using a digital hand-held refractometer with a dynamic control system (RFM340 + BS®, Bellingham and Stanley Ltd, Basingstoke, Hants, UK) and TA was determined by mixing 10 mL juice with 50 mL distilled water and titrating with 0.1 M sodium hydroxide (NaOH) to the end point (pH of 8.1). The volume of NaOH titrated to endpoint was recorded and TA was calculated using the citrus acid formula (Eq. 8) and was expressed as  % citric acid.

TA%citricacid=0.0064×titreNaOHmL×10010mLjuice 8

Extraction of total phenolics and flavonoids

The concentration of total phenolics was spectrophotometrically determined using a method described by Ilahy et al. (2011) with modifications. Briefly, 150 ± 0.5 mg was extracted with 3 mL of 80% methanol. The solution was vortexed for 1 min followed by centrifuging for 10 min using GenVac® (SP Scientific, Genevac LTD., Suffolk, UK). For extraction of total phenolic content, 50 µL was poured into a test tube and diluted with 950 µL of distilled water. This was followed by the addition of 125 µL Folin–Ciocalteu reagent. After 3 min, the addition of 1250 µL 7% sodium carbonate solution followed, and distilled water was used to make up the final volume to 4 mL. The solution was incubated in the dark at room temperature for 90 min. The absorbance was measured at 760 nm against blank and the results were expressed as g gallic acid equivalent per kg (g/kg GAE).

For the determination of total flavonoid concentration, the aluminum chloride colorimetric assay described by Kamtekar et al. (2014) was used. Briefly, 500 µL of the diluted solution was added with 4 mL and 300 µL of 5% sodium nitrate solution. This was allowed to stand for 5 min then followed by the addition of 300 µL 10% aluminum chloride. After 6 min, 2 mL of 1 M sodium hydroxide was added. Distilled water was added to give a final volume of 10 mL and this gave rise to orange to yellowish color. Using a spectrophotometer, the absorbance was measured at 510 nm against the blank. All samples were measured in triplicates and results for flavonoids were expressed as g of quercetin equivalents per kg of dry mass (g/kg QE).

Extraction and quantification of rind ascorbic acid

Ascorbic acid was extracted from the freeze dried sample using a method described by Hernández et al. (2006) which was slightly modified for citrus. Briefly, 150 ± 0.5 mg of the dry sample was mixed with 5 mL of 3% (w/v) aqueous metaphosphoric acid. The solution was homogenized for 1 min using a vortex, and then placed in ice cubes for 5 min. The sample was thereafter centrifuged for 20 min using GeneVac (SP Scientific, Genevac LTD., Suffolk, UK) with lamp off. Subsequently, 0.5 mL was incubated in the dark using 2.5 mL of 2.6 dichloroindophenol dye (0.015 g dye in 100 mL of H2O). The reading of the absorbance was at 515 nm in triplicates and the results were expressed as g/kg on dry weight basis.

Statistical analyses

The data for all variables measured was subjected to the analysis of variance (ANOVA) using GenStat statistical software (GenStat®, 18th edition, VSN International, UK). Means were separated using least significance differences measured at p ≤ 0.05.

Results and discussion

Effect of coating treatment and canopy position on peteca spot

The development of peteca spot was significantly affected by the interaction between coating treatment and canopy position (p < 0.001) (Fig. 1a). In this study, fruit were systematically harvested from two canopy positions, namely, the sun exposed outside canopy position (OC) and inside canopy (IC). This is because fruit are produced throughout the canopy around the tree and are exposed to varying irradiation and temperature which may result in difference in color of fruit from the same tree (Cronje et al. 2013). The major influence caused by this difference is the effect it has on consumer preference with regard to eating quality, physical appearance and the development of physiological disorders in citrus fruit (Magwaza et al. 2013).

Fig. 1.

Fig. 1

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Effect of edible coatings (a), canopy position (b) on peteca spot incidence and mass loss (c) of ‘Eureka’ lemon fruit harvested from inside canopy (IC) and outside canopy (OC) positions and stored at 3 °C for 12 weeks. LSD least significance difference, CP canopy position, CT coating treatment

The effectiveness of the coating treatments was demonstrated by the difference in peteca spot development between the coated and control fruit in the same canopy position. The control fruit had the highest incidence of the disorder (16.5%) compared to fruit coated with M + CH (6.5%), CMC (1.6%), CH (4%) and M + CMC (0.6%) and this was exacerbated on fruit harvested from the inside position of the tree canopy compared to the outside canopy (Fig. 1a). Fruit coated with CH, CMC and M + CMC coatings were less susceptible to peteca spot development throughout the storage time irrespective of canopy position. The coatings probably inhibited the degeneration of oil glands, a key phenomenon in PS development. Moreover, it could be hypothesized that, compared to other coatings, M + CMC allowed sufficient gaseous exchange thereby reducing CO2 accumulation around the fruit, which is a well-known cause of PS.

The effectiveness of CH coating in reducing chilling injury and preserving quality of cucumber was also demonstrated by Zhang et al. (2015). Another observation made was that fruit harvested from the outside canopy had less peteca spot development compared to fruit in the inside canopy. Comparable results were also reported by Magwaza et al. (2013) and Cronje et al. (2013) where ‘Nules Clementine’ mandarin harvested from shaded position inside the tree canopy had higher rind breakdown than those from outside sunexposed position. This has been largely attributed to sunlight exposure of the fruit while they are still attached to the tree, which maximizes the respiration and photosynthesis processes, hence increasing fruit’s biochemical attributes including non-structural carbohydrates and antioxidants that protect the fruit from any stress that leads to the development of physiological disorders such as rind breakdown disorder, chilling injury and PS (Cronje et al. 2013; Magwaza et al. 2013).

The interaction between storage time and canopy position was not significant (p = 0.054), however, storage time was highly significant (p < 0.001). This could be due to the fact that of the all coating treatments, control had a high incidence of the disorder while CMC, M + CMC and CH showed less susceptibility throughout storage time. The PS index was low during the first 3 weeks of cold storage followed by a rapid increase from week 6 (Fig. 1b). This shows that peteca spot may not occur directly after harvest and its development may coincide with the time the fruit reach the international market causing a huge economic loss for the citrus industry.

The effect of coating treatments and storage time on mass loss of ‘Eureka’ lemon

The significant interaction between coating treatment and storage time (p < 0.001) defined the changes in mass loss over 12 weeks of cold storage at 3 °C. From the results observed, coating treatments were effective in reducing mass loss over time compared to the control (Fig. 1c). Fruit coated with M + CMC had the least percentage of mass loss (9.77%) after the storage period followed by CH and CMC, with mass loss of 10.6 and 14.0%, respectively. This shows the ability of the coating to maintain the initial mass of fruit during cold storage at 3 °C. The explanation for the coating’s ability to reduce mass loss could be because coatings, such as chitosan when applied to the fruit, have the ability to form a film on the fruit surface which blocks water vapor exchange hence reducing water loss through the process of transpiration (Shao et al. 2015).

Carboxymethyl cellulose coating has been reported to form a semipermeable layer on the fruit surface which reduces moisture loss, respiration as well as the movement of solutes across membranes (Arnon et al. 2015). A delay in mass loss is one of the main benefits of applying coatings in fruit mainly because of the barrier they form which reduces oxygen supply. The importance of fruit mass is seen on a daily basis in local stores where the mass of the fruit determines its price. Fruit are usually sold per kg and fruit that show shrinkage are discarded. This makes it important for the fruit to maintain its mass throughout storage time and shelf-life in order to minimize losses, not only in the local markets but in the export market as well.

Although the coatings were found effective in reducing mass loss, fruit coated with M + CH had a high increase in mass loss following the trend for control (uncoated fruit). At the end of storage, M + CH coated fruit lost about 21.63% of the initial mass while control fruit loss about 24.17%. The results found in this study corroborate with those previously reported by Chien and Chou (2006) where the application of chitosan edible coating was effective in controlling the postharvest quality of Tankan fruit, by reducing mass loss and ascorbic acid loss.

Canopy position had no significant effect on the initial mass of fruit, however, the mass started changing with time (Table 1). This could be due to water loss by the fruit through active metabolic processes like respiration and transpiration under cold storage. A change in the water status of the rind is commonly known as one of the determining factors for fruit susceptibility to rind pitting disorder, hence control fruit that showed a higher percentage of mass loss were more susceptible to peteca spot.

Table 1.

Physicochemical and phytochemical quality parameters of ‘Eureka’ lemon in fruit harvested from inside canopy and outside canopy positions and stored at 3 °C for 12 weeks

Storage time (weeks) Inside canopy Outside canopy
Mass (g) TSS (%) TA (%) Tcar (g/kg) Phenols (g/kg GAE) Flavonoids (g/kg QE) Mass (g) TSS (%) TA (%) Tcar (g/kg) Phenols (g/kg GAE) Flavonoids (g/kg QE)
0 122.6ab 5.23a 2.63a 41.52a 1.65a 2.13b 127cde 6.2a 3.52b 64.1a 2.24b 2.46cd
3 106.71a 5.31b 3.25ab 69ab 2.88cd 2.19b 120.1bcd 5.9b 3.25a 73.74ab 2.15b 2.49cd
6 107.1a 6.5b 4.85bc 91.21abc 3.06d 2.63d 119bc 6.8ab 4.98ab 133.62cd 2.33b 2.96e
9 118.21bc 6.07ab 5.81d 103.21bc 1.63a 1.98b 130.7e 7.2c 5.79bc 128.61d 2.80cd 1.37a
12 110.81ab 7.12c 5.25cd 157.12d 1.58a 2.28bc 129.9de 7.8cd 5.11b 237.41e 2.75c 1.63a
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Mean values with different letter (s) in the same column indicate statistically significant differences (p < 0.05) according to Duncan’s multiple range test

TSS total soluble solids, TA titratable acidity, Tcar total caroteniods

The effect of coating treatments and canopy position on color and total carotenoids

Coating treatments significantly affected the fruit color parameters (p < 0.001). Amongst the treatments, control fruit were more luminous with values ranging from 81.11 after harvest to 92.79 at the end of storage time (Fig. 2a). This was followed by M + CH coated fruit with values ranging from 83.05 to 93.49. Although the change in color for all the treatments followed the same trend, control and M + CH treatments showed a rapid loss of the initial green color such that by the third week of cold storage, the fruit had already developed shades of yellow color on the rind which turned completely yellow by the end of storage time (data not shown).

Fig. 2.

Fig. 2

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Effect of coating treatments on color parameters (luminosity (a); greenness (b); yellowness (c); citrus color index (d)) of fruit harvested from outside canopy (OC) and inside canopy (IC) positions over 12 weeks of postharvest cold storage at 3 °C. LSD least significance difference, CP canopy position, CT coating treatment

These results demonstrated the effectiveness of edible coatings in delaying color degradation and maintaining the lower values of L*, a* and b*. The edible coatings (CH, CMC and M + CMC) were effective in maintaining the initial green color by inhibiting a fast chlorophyll degradation (Fig. 2b). Ali et al. (2011) ascribed a delay in color change to low respiration and reduced ethylene which results in a modified fruit atmosphere. This could explain the very low peteca spot incidence in coated fruit since the color change was slow, because yellow fruit are more susceptible to PS than green fruit (Undurraga et al. 2009).

Edible coatings are known to create a semipermeable film which is able to delay ripening and senescence and inhibits color alterations (Han et al. 2014) of which the three treatments (CH, CMC and M + CMC) were able to do. The loss in green color as the fruit changes to yellow can be related to ethylene production which causes a natural ripening process which is also related to chlorophyll breakdown and an increase in carotenoids content. The relationship between coating treatments and color change in fruit is through delaying metabolic processes that lead to a rapid increase in color change. Han et al. (2014) reported a retention in color after the application of chitosan in gourd. Chitosan coating was also found to delay ripening in guava (de Aquino et al. 2015).

The color of the fruit was significantly affected by canopy position (p < 0.001). Sun exposed fruit from outside canopy had high luminosity (L*), greenness (a*) and yellowness (b*) which shows a better color development compared to the fruit harvested from inside position of the tree canopy. However, a rapid increase in color change for control and M + CH was observed with L* values reaching 87.94 and 87.35 respectively and yellowness 62.59 and 61.64 respectively while in the other coatings luminosity ranged from 83.01 to 85.67 and yellowness 58.41–59.49. The low values of greenness in the inside canopy fruit coated with (CH, CMC and M + CMC) (Fig. 2b) demonstrate the ability of coating to delay breakdown of chlorophyll and the synthesis of carotenoids. The low color change in the inside canopy could be caused by the reduced intensity of sunlight reaching the fruit while still attached to the tree hence reducing metabolic processes in the fruit during storage.

The application of coatings in fruit delays color breakdown and the synthesis of carotenoids. The loss in pigment content which contributes to a change in green color is due to the conversion of chloroplast to chromoplasts leading to a fast ripening and the formation of lycopene and β carotene (Ullah et al. 2017). Mature citrus fruit are known to contain chromoplasts with the ability to store huge amounts of carotenoids which could explain why carotenoids were increasing as the fruit ripens (Table 1). The chromoplast usually shows natural variations in the type and level of accumulation of carotenoids amongst same species. Coating treatments caused a significant effect on total carotenoids (p = 0.002). Fruit coated with M + CMC showed high carotenoids in the outside canopy compared to the rest of the treatments which can be related to the color index (Fig. 3b).

Fig. 3.

Fig. 3

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Effect of edible coatings on citrus color index (a), total carotenoids (b), β carotene (c) and lycopene (d) of ‘Eureka’ lemon fruit harvested from inside canopy (IC) and outside canopy (OC) positions during postharvest cold storage of 3 °C. LSD least significance difference, CP canopy position, CT coating treatment

Carotenoids have an advantageous ability to prevent membrane damage because they play a role as photoprotective compounds in fruits (Cronje et al. 2011). This could be the reason why coatings that had high carotenoids (M + CMC, CMC and CH) were less susceptible to PS incidence. Canopy position also showed a significant effect in total carotenoids (p < 0.001). Fruit harvested from the outside canopy had more carotenoids compared to those in the inside canopy with values ranging from 118 to 145 g/kg in the inside canopy and 75–114.5 g/kg in the inside canopy (Fig. 3b). This is because light is an important factor in the synthesis of carotenoids.

Coating treatments had no significant effect on β carotene, however, canopy position significantly affected the concentrations of β carotene and lycopene (p < 0.001) (Fig. 3c, d). Fruit harvested from outside canopy had the highest β carotene ranging from 5.1 to 5.8 g/kg while fruit from the inside canopy had 3.9–4.6 g/kg B carotene. β carotene is one of the pigments found in citrus fruit that plays a role in plant’s metabolism and photosynthesis. An increase in lycopene concentration is dependent on the color of the fruit. The ripeness, as well as the developmental conditions of the fruit is associated with an increase in lycopene (Abdel-Salam 2016).

The control treatment showed a rapid increase in lycopene during the first weeks of storage which gradually decreased over time from 14.85 to 10.82 g/kg. This could be due to the fact that control fruit started changing color from the early stages of storage and the fruit were reaching senescence at a faster rate. The synthesis of lycopene is affected by storage time and modification of the atmosphere and this is because under cold storage conditions, the metabolic activity of the fruit is reduced resulting in decreased physiological changes in the fruit (Abdel-Salam 2016). An increase in β carotene and lycopene in the sun-exposed fruit can be related to increased radiation and temperature which plays a role in pigment production. Lycopene is known to play a role in the color development of citrus fruit meaning that fruit with high lycopene concentration in the outside canopy position had a better color development.

The effect of coating treatments on TSS and TA

The results showed that neither coating treatment nor canopy position had a significant effect on total soluble solutes (TSS) and titratable acidity (TA) (Table 1). This coincides with the observation that was found by Machado et al. (2012) where the application of coatings had no effect on physicochemical properties and in cases where there was a difference, the difference was not significant between the coated and uncoated fruit. Olarewaju et al. (2018) also found canopy position to cause no significant effect on TSS of ‘Marsh’ grapefruit, however, the authors reported TA and TSS/TA to be significantly affected by canopy position where outside canopy fruit had high TA compared to inside canopy fruit.

Total acidity is strongly associated with the ripening and has long been used in maturity indexing of various horticultural products (Obenland et al. 2008). For non-climacteric fruit like lemon, there are no considerable alterations after harvesting the fruit which could be the reason why there were no significant chemical variations during storage time, hence coating treatments and canopy position caused no difference. Obenland et al. (2008) also reported that coatings did not cause any significant effect in TSS and TA of ‘Navel’ oranges stored at 5 °C for 6 weeks. The titratable acidity in this study was found to be highly influenced by storage time (p < 0.001). The values of TA during storage increased from 2.63 to 5.25% at the end of storage (Table 1).

Some authors have observed a decline in TSS and TA of fruit that were not coated which was also related to weight loss and respiration rate (Toǧrul and Arslan 2004). The decrease is caused by a reduction in respiration rate which decreases the synthesis and the use of metabolites thereby resulting to a decrease in TSS through slower hydrolysis of carbohydrates to sugars (Obenland et al. 2008). In a study conducted in guavas, de Aquino et al. (2015) found an increase in TSS of uncoated fruit meaning the fruit ripened faster hence the quality of the fruit was altered. This was also found to be true in uncoated grapes (Sánchez-González et al. 2011).

The effect of coating treatment and canopy position on phenolic and flavonoid concentrations

One of the important roles of phenolic compounds in plants is in helping the plant defend itself against pests and diseases. The health promoting characteristics that have been reported in citrus fruit are known to be dependent on phenolics and flavonoids concentrations (Lü et al. 2016). The results showed that phenolics were significantly affected by coating treatment (p < 0.001). Fruit coated with M + CMC had more phenolic concentration while control showed a low concentrations (Fig. 4a, b). Phenolics were also significantly affected by storage time (p < 0.001). This could be due to the polyphenol oxidase activity which is known for causing phenols oxidation after a certain period of time.

Fig. 4.

Fig. 4

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Effect of coating treatments and their combined effect with storage time on phenolic (a and b) and flavonoids (c and d) concentration of ‘Eureka’ lemon fruit during 12 weeks postharvest cold storage at 3 °C. LSD least significance difference, CP canopy position, CT coating treatment; RP rind position, ST storage time

This study evaluated phenolics and flavonoids in two different rind positions, the flavedo and the albedo which were found to be significantly different (p < 0.001). To the best of our knowledge, the amount of phenolic and flavonoid concentrations in the flavedo and albedo of ‘Eureka’ lemon has not been evaluated before. This is because citrus rind has been the most ignored part of the fruit while it contains considerable amount of flavonoids and phenolics (Lü et al. 2016). Phenolics are important in plants because they help defend the plant from stress conditions and adapt to abrupt changes in environmental conditions (Ćetković et al. 2007). From the results, it was found that phenolics were more abundant in the albedo while flavonoids were more in the flavedo (Fig. 4a, c). Similar results were observed by Lü et al. (2016) in Pummelo fruit. However, Escobedo-Avellaneda et al. (2014) found that both phenolics and flavonoids were more abundant in the albedo than in the flavedo of ‘Valencia’ orange. The concentration of phenolics in the albedo had values ranging from 2.153 to 2.691 g/kg GAE and 1.830–2.152 g/kg GAE in the flavedo.

There was a slight difference in coating treatments with M + CMC, M + CH, CH, CMC and control reaching values of 2.691, 2.528, 2.491, 2.354 and 2.153 g/kg GAE, respectively, at the end of storage time (Fig. 4b). However, control fruit showed a rapid decrease in total phenols which started 6 weeks after storage. Dong et al. (2019) evaluated the total phenolics in ‘Eureka’ lemon peels and found that the highest concentration was 7.960 g/kg GAE while the lowest was 4.300 g/kg GAE which is higher than what was found in this study, probably because their extraction was done on fresh weight. Irkin et al. (2015) found the highest concentration in lemon to be 5.810 g/kg GAE.

Rind position caused a significant effect on total flavonoid concentration (p < 0.001). Unlike phenolics, flavonoids were found to be more abundant in the flavedo than in the albedo. The total flavonoid concentration in the flavedo ranged from 2.104 to 2.907 g/kg QE and 1.872–2.104 g/kg QE in the albedo (Fig. 4c). Flavonoids were also found to be significantly affected by coating treatments (p < 0.001) and high values were observed in the flavedo of fruit coated with CMC, while low values were found in fruit coated with M + CH (Fig. 4d). Previous studies have demonstrated that postharvest treatments and practices have enormous influence on the metabolism of flavonoids (Rodrigues et al. 2010). In this study, it could be argued that coating the fruit with CMC positively affected flavonoid metabolism. The reduced flavonoid concentration under other coating treatments warrants further investigation.

The type of fruit and storage conditions may have a huge influence on the concentration of phenols and flavonoids. This partially explains why there was a huge variation amongst the concentration of phenolic and flavonoids in citrus fruit. Phenolics are known as secondary metabolites that play a role in functioning of living cells and are important for scavenging free radicals. The high variation in these concentrations could be due to the difference in cultivars, extraction methods, coating treatments, environmental and growing conditions. Storage period has also been reported to influence the concentration of phenolics and flavonoids which could also explain the results found in this study. This is because under low storage conditions, the activities and transcriptional activators that play a role in the synthesis of phenolics and flavonoids are affected (Zou et al. 2016).

Both phenolic and flavonoid concentrations were significantly affected by canopy position (p < 0.001). More concentrations were found in the outside canopy than inside canopy. Comparable results were reported by Olarewaju et al. (2018) in ‘Marsh’ grapefruit. Ben-Yehoshua et al. (1992) explained the reason of high concentration of phenolics in the outside canopy to be related to the high radiation that stimulates the production of phenylalanineaminialyase inducing the production of phenolic compounds. This is also related to the high photosynthetically active radiation in the outside canopy which initiates phytoalexins synthesis, a phenolic compound that helps the fruit defend itself against stress conditions (Ben-Yehoshua et al. 1992).

Hagen et al. (2007) also related a high production of phenolic concentration to high radiation from the sunlight in the outside canopy position of the tree. Similarly, the synthesis of flavonoids has also been reported to be related to light intensity and temperature (Treutter 2001). The enzymes that are involved in the production of flavonoids are stimulated by light hence the concentration increases in sun-exposed fruit (Treutter 2001). This could explain the high concentration of phenolics and flavonoids that were observed in fruit harvested from outside canopy.

The effect of coating treatments and canopy position on ascorbic acid

The concentration of ascorbic acid (AsA) in citrus is a determining factor for fruit quality and shelflife (Laing et al. 1978). The stored fruit reaches senescence more quickly when there is a rapid loss of ascorbic acid and this makes it important to find ways to delay the loss which is done through the application of edible coatings. Coating treatments had a significant effect (p < 0.001) on ascorbic acid of ‘Eureka’ lemon (Fig. 5a, b). Amongst the treatments, control and M + CH had low concentrations of ascorbic acid, 1.08 and 1.12 g/kg, respectively, and the loss rate was faster during storage time compared to the other treatments (Fig. 5a). This was seen by the fast decline in the concentration after 6 weeks of cold storage (Fig. 5b). Fruit coated with CH, CMC and M + CMC had AsA concentration of 1.75, 1.60 and 1.59 g/kg, respectively. These coating treatments were effective in reducing AsA loss which could partly explain the lower susceptibility of coated fruit to peteca spot.

Fig. 5.

Fig. 5

Open in a new tab

Effect of coating treatments (a) as well as their combined effect with storage time (b) on ascorbic acid of ‘Eureka’ lemon harvested from inside canopy (IC) and outside canopy (OC) positions and stored for 12 weeks at 3 °C (b). LSD least significance difference, CP canopy position, CT coating treatment, RP rind position, ST storage time

The results showed that ascorbic acid was significantly affected by canopy position; rind position and storage time (p < 0.001). The outside canopy fruit had high concentration of ascorbic acid compared to the inside canopy fruit mainly because of the high exposure of the fruit to sunlight during growth and development (Fig. 5a). Comparable results were reported by Ncama et al. (2018) where ‘Marsh’ grapefruit harvested from the outside canopy had high concentration of ascorbic acid compared to inside canopy fruit. The high concentration of AsA in the outside canopy can be related to the high carbohydrates that were also observed in the outside canopy because AsA is synthesized from carbohydrates (Valpuesta and Botella 2004). A high AsA can also be related to defense mechanism of fruit against stress conditions (Laing et al. 1978).

The average concentration of ascorbic acid was more in the flavedo (1.60 g/kg) than the albedo (1.30 g/kg) part of the fruit in the outside canopy position. While fruit in the inside canopy had an average of 1.56 k/kg in the flavedo and 1.12 g/kg in the albedo. The separation of the flavedo and albedo was done to compare the difference in the two tissues since PS is known to not only affect the flavedo but also the albedo. The interaction between canopy position and rind position was found to be significant (p < 0.001), indicating that the difference in concentrations within the rind position was affected by the position of the fruit while still attached on the tree. Ascorbic acid was also found to change over time during cold storage. Storage time, storage temperature and light are some of the factors that lead to the degradation of ascorbic acid. Burdurlu et al. (2006) found about 52.8% AsA loss in lemon after 8 weeks of cold storage. Ascorbic acid is well known for being highly unstable and it easily decomposes and changes over time, especially during unfavorable storage conditions.

These results confirm those found by Adetunji et al. (2013) where moringa incorporated with CMC was effective in reducing AsA loss during cold storage in citrus fruit. The mechanism behind this, as explained by the authors is due to the low oxygen permeability of the coating treatment which was able to lower the activity of the enzymes that are responsible for the oxidation of AsA. Shao et al. (2015) evaluated the effectiveness of chitosan and clove oil edible coatings on citrus green mould and found that pure chitosan prevented the growth of green mould while the combination of the two was not effective and as found in this study, fruit coated with M + CH coating was not effective in delaying or reducing AsA loss. A delay in AsA loss by chitosan was also observed by Ali et al. (2011) in papaya fruit. Similarly, the application of CMC was also found to reduce AsA loss in mandarin fruit (Toǧrul and Arslan 2004) which is due to the gas barrier of the coating that inhibits oxygen from entering the fruit hence decreasing the possibility of AsA autoxidation in aerobic conditions.

Conclusion

This study demonstrated the effectiveness of edible coatings in reducing the incidence of peteca spot of ‘Eureka’ lemon during cold storage. The results showed that fruit coated with M + CMC, CMC and CH were less susceptible to the development of the disorder in fruit from both inside and outside canopy positions while the control showed a high incidence of the disorder followed by M + CH coating. The incidence of peteca spot was not only affected by coating treatments but storage time and canopy position also played a role. Fruit from the inside canopy position were found to be more susceptible to the development of the disorder compared to fruit harvested from the outside canopy. To conclude, the study demonstrated the potential of M + CMC, CH and CMC edible coatings as the best postharvest treatments for reducing peteca spot in ‘Eureka’ lemon. The most effective coating treatment was moringa incorporated with carboxymethyl cellulose (M + CMC) followed by pure CMC and pure chitosan (CH). These coating treatments were also able to reduce ascorbic acid loss, mass loss and a delay in color change which prevented the fruit from ripening fast and reaching senescence. Either one of the coatings (M + CMC, CMC or CH) is therefore, recommended for coating fruit before packing and distribution. The combination of moringa and chitosan (M + CH) was less effective in reducing the incidence of peteca spot, therefore the coating is not recommended.

Acknowledgements

This research was financially supported by Citrus Academy and National Research Foundation of South Africa. The authors are grateful to Mr. Thokozani Nkosi for his technical assistance in the Postharvest Research Laboratory of the University of KwaZulu Natal, Pietermaritzburg.

Footnotes

Publisher's Note

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Contributor Information

Lembe Samukelo Magwaza, Email: magwazal@ukzn.ac.za.

Asanda Mditshwa, Email: mditshwaa@ukzn.ac.za.

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