Open access peer-reviewed chapter

Quality of Postharvest Degreened Citrus Fruit

Written By

Julia Morales, Lourdes Cervera, Pilar Navarro and Alejandra Salvador

Submitted: 12 April 2022 Reviewed: 02 May 2022 Published: 04 July 2022

DOI: 10.5772/intechopen.105119

From the Edited Volume

Citrus Research - Horticultural and Human Health Aspects

Edited by Mateus Pereira Gonzatto and Júlia Scherer Santos

Chapter metrics overview

260 Chapter Downloads

View Full Metrics

Abstract

External color is a key factor that defines external citrus fruit quality. Degreening with exogenous ethylene exposure is a widely used postharvest treatment applied to promote external citrus fruit color development, mainly with those cultivars that reach internal maturity while their external peel color is still green. Ethylene plays a crucial role in the color change of citrus fruit because it induces two simultaneous, but independent, processes—chlorophyll degradation and carotenoid synthesis. However, it is important to know, in addition to the effect on skin color development, whether this treatment can negatively affect other fruit quality parameters. This chapter addresses the influence of postharvest degreening treatment on the physicochemical, nutritional, and sensory quality of citrus fruit.

Keywords

  • ethylene
  • color
  • biocomponents
  • antioxidant
  • disorders
  • flavor

1. Introduction

External citrus fruit color is an important quality attribute to be considered for the fresh market. Consumers associate high-quality fruit with the typical bright orange skin color, while they associate greenish skins with unripe fruit [1].

In citrus fruit, color change requires not only night temperatures close to 12°C but also marked differences between day and night temperatures. At 12°C, the expression of the key genes of the carotenoid biosynthesis pathway is stimulated, which increases concentrations of carotenoids and xanthophylls [2]. However, in tropical countries without cold night temperatures, citrus fruit reaches acceptable internal quality without displaying the characteristic orange color, and fruit is consumed when the skin is yellowish-green.

In Mediterranean citrus production areas, early citrus varieties, especially mandarins and oranges, reach internal maturity before full external coloration. In these cases, a degreening treatment, with the application of exogenous ethylene, is a common postharvest practice followed to improve external fruit color, which contributes to their market acceptance and extends their marketing season. Moreover, in mature citrus fruit harvested after the color break, it has been reported that exogenous ethylene can reduce the incidence of important postharvest physiological disorders, such as non-chilling peel pitting or chilling injury [3, 4]. These disorders are manifested as peel damage, as well as the incidence of the disease caused by Penicillium digitatum without negatively affecting fruit organoleptic properties [3, 5].

The degreening treatment applied to enhance external citrus fruit color involves exposing the fruit to low ethylene concentrations [6]. However, in addition to ethylene concentration, other important factors, such as temperature, humidity or carbon dioxide (CO2), and oxygen in the atmosphere, are implied during color change. The exhaustive control of all these factors, as well as the process duration, are requirements to achieve the desired external color without promoting undesirable reactions related to physiological disorders or sensory changes, which harm fruit quality during their posterior shelf-life.

This chapter describes the parameters involved in the degreening process, and its impact on external or internal fruit quality.

Advertisement

2. Factors involved in the postharvest degreening process

In climacteric fruit, ethylene plays a key role in governing physiological and biochemical changes that occur during ripening, including the color break, softening, and accumulation of sugars, acids, aroma volatiles, and vitamins [7]. In contrast, citrus fruit is non-climacteric, and their natural ripening is not accompanied by rises in respiration and ethylene production rates [8]. However, exposure to exogenous ethylene has been shown to stimulate various ripening-related processes, such as destruction of the green chlorophyll pigments and accumulation of orange/yellow carotenoids, in citrus peel tissue. Exogenous ethylene increases chlorophyllase activity and gene expression as well as other genes involved in chlorophyll breakdown [9, 10]. Ethylene also down-regulates chlorophyll biosynthesis, by repressing the gene expression of Mg-chelatase and most genes involved in photosynthesis and chloroplast biogenesis [11]. Ethylene also stimulates the transcription of carotenoid biosynthetic genes in citrus fruit peel, which is concomitant to both the transformation from chloroplast into chromoplast and the accumulation of xanthophylls and carotenoids [11, 12]. Therefore, degreening treatment with exogenous ethylene exposure is a widely used postharvest treatment to promote external color development in citrus, especially in those cultivars that reach internal maturity while external peel color is still green [12, 13].

Commercial postharvest degreening is usually carried out in packinghouses, specifically in temperature-controlled chambers equipped with automatic injectors to provide the appropriate ethylene concentration. The applied ethylene concentration is low, close to 1–5 ppm [14, 15]. This concentration suffices to cause a color change, and it has been reported that increasing ethylene concentration has no significant effect on improving peel color or reducing degreening times [16]. Exposing citrus fruit to higher ethylene concentrations can cause undesirable effects related to accelerated fruit senescence. It is, therefore, necessary to monitor ethylene levels constantly throughout the process to ensure that its concentration is sufficient for proper degreening without detriment to quality.

Temperature is a determinant of color evolution during the ethylene degreening process. Temperature strongly influences chlorophyll degradation and carotenoid synthesis. High temperatures close to 30°C lead to rapid chlorophyll loss but delay carotenoid accumulation. However, the temperature within the 18–20°C range allows greater carotenoid accumulation, although chlorophyll degradation is slower. Very low temperatures (close to 5°C) during the process can repress carotenoid accumulation and affect carotenoid composition in flavedo [17]. In Spain, mandarins are subjected to degreening treatment at 18–21°C, while oranges are exposed to a slightly higher temperature of 20–22°C [18]. However, the degreening of lemons is carried out at 25–30°C [19]. Similarly in Israel and California, mandarins and oranges are exposed to 20–25°C [20, 21, 22]. In Florida, most citrus fruits are commercially degreened at a relatively high temperature of 28–29°C [23].

Another important factor to consider in the degreening treatment is the time required to reach the desired fruit color, which very much depends on both the cultivar and the initial fruit color which, in turn, are controlled by fruit maturity and orchard conditions [18]. Citrus peel color increases with the ethylene exposure time during the degreening process. However, the negative effects induced by ethylene are also stronger the longer the exposure time is. Therefore, the time during which fruit is exposed to ethylene should be as short as possible, and optimal temperature, ethylene concentration, humidity, and aeration condition should apply. Not exceeding 72–96 h of treatment is advisable to avoid peel disorders during posterior commercialization [24]. Current color sorters, which work with photoelectric cells on handling lines, allow the fruit to be selected according to their initial color and to adjust degreening treatment duration to avoid overexposing fruit to ethylene. It should be noted that fruit color evolution continues once the fruit is transferred from ethylene chambers to marketable conditions [6]. However, the temperature to which fruit is subjected after the degreening treatment is key for posterior color evolution. Color development can be limited if temperatures are low while shipping citrus fruit [25]. The combination of periods with and without ethylene exposure has successfully achieved the desired change in mandarins and oranges, and optimal ethylene exposure duration has been estimated by considering color at harvest and subsequent marketing conditions [6]. In addition, the color change that fruit undergoes during degreening treatment very much depends on the variety [6, 24, 26].

Exposing fruit to ethylene increases the fruit respiration rate inside degreening chambers [27]. CO2 is known as an ethylene antagonist which, at high concentrations, inhibits the action of ethylene and delays the color change process. Therefore, the chambers in which degreening is carried out must be equipped with specific CO2 sensors to continuously monitor its concentration. CO2 must be kept below 0.15–0.2% to allow proper degreening. High CO2 levels in the atmosphere may induce acetaldehyde and ethanol production with the consequent risk of off-flavors in fruit [20]. The oxygen concentration has to remain above 20% because, apart from its role in respiration activity, oxygen is necessary for chlorophyll degradation and carotenoid biosynthesis. Therefore, adequate ventilation is essential to supply oxygen and remove CO2 accumulation in degreening chambers. Moreover, during degreening treatments, keeping relative humidity at around 95% is desirable to obtain satisfactory peel color change results and to avoid fruit dehydration and skin alterations [28].

Advertisement

3. Physiological disorders

Apart from the benefits that exogenous ethylene application during degreening treatment can provide to improve fruit coloration, it can lead to physiological alterations in fruit if the process is not properly carried out.

The negative effects associated with exposing the fruit to exogeneous ethylene are related to an accelerated senescence process, which can lead to major quality loss and a shorter shelf-life [26, 29]. These undesirable effects depend mainly on the concentration and duration of fruit exposure to ethylene, but also affect atmospheric conditions, such as low humidity, excessive temperature, and high CO2 concentrations. The incidence of these alterations also depends on the cultivar, preharvest conditions, and the treatment of the postharvest condition. In most cases, these disorders do not appear immediately after the degreening process but are manifested later during storage until marketing [16]. Special care must be taken when fruits are to be shipped at low temperatures, which occurs with exports to countries with quarantine requirements because low temperatures after degreening can accelerate the manifestation of these alterations. Therefore, to avoid possible fruit disorders, treatment must be carried out under careful conditions by considering all the factors involved in the process, as well as the conditions to which fruit are subjected after degreening.

The most frequent physiological disorders associated with incorrect degreening treatment are described below.

3.1 Calyx senescence

Calyx drop and browning are the main physiological disorders associated with incorrect degreening (Figure 1). Keeping the calyx fresh during the postharvest life of citrus fruit is a quality requirement because fruits are commercially more attractive, and it also protects the fruit from fungal infection upon abscission [30].

Figure 1.

Calyx senescence. Browning and drop of the calyx.

Ethylene is a vegetal hormone that promotes tissue abscission and senescence in fruit [31]. Low atmospheric ethylene levels (≤0.01 μL/L) reduce this disorder during long-term storage, and its accumulation during cold storage has been related to calyx senescence [32].

During degreening treatment, ethylene application has been reported to increase the activity of both polygalacturonic acid enzyme (PG) and cellulase (Cx), which promote browning and calyx abscission [33]. The incidence of calyx senescence triggered by degreening depends mainly on the ethylene concentration and process duration [26, 30, 34], and it is also very cultivar dependent. Clementine mandarins ‘Marisol’ and ‘Oronules’ have been shown to be more sensitive to calyx senescence than ‘Clemenpons’ and ‘Clemenules’ [35]. Other citrus cultivars, such as ‘Satsuma’ mandarin and ‘Navelina’ orange, are extremely sensitive to calyx senescence [6, 26]. Despite these calyx disorders appearing sometime after degreening, their incidence is accentuated with post-treatment storage time.

Many studies have focused on finding solutions to prevent calyx senescence during degreening. Using auxins has been one of the effective treatments in controlling this alteration. Synthetic auxin 2,4-dichlorophenoxyacetic acid (2,4-D) has been extensively reported as a treatment to retard calyx abscission, drying, and browning. It occurs as a consequence of exposing the fruit to ethylene during degreening treatment [30, 34, 36]. This auxin’s mechanism of action is to reduce PG and Cx activities and to increase the lignin and water contents of fruit peel [37]. Despite this auxin having been widely employed and proving useful, it has been restricted by current European Union legislation, hence the need to find other synthetic auxins to avoid physiological changes in the calyx [33, 35].

Carvalho et al. [35] tested four synthetic auxins (2,4-dichlorophenoxy propionic acid (2,4-DP); 3,5,6-trichloro-2-pyridyloxyacetic acid (3,5,6-TPA); 2,4-D isopropyl ester; 2,4-D-amine) for retarding the calyx disorders caused by degreening in different clementine cultivars. All the evaluated auxins reduced calyx senescence. In all the cultivars, the best results were obtained by applying 3,5,6-TPA, followed by 2,4-D isopropyl ester. In contrast, the treatment with 2,4-DP had a positive effect on avoiding calyx disorders, but only in ‘Clemenpons’ mandarins, and this effect was not observed in the other studied cultivars. Although auxin treatments can delay color evolution, they had no negative effect from a commercial point of view in all the studied cultivars because, after degreening, all the treatments had a commercially acceptable color index. Moreover, no auxin treatment affected the sensory quality of degreened fruit.

The application of 3,5,6-TPA at different concentrations (10, 20, and 40 ppm) under commercial degreening conditions has been well-studied with many varieties. The higher the 3,5,6-TPA dose, the lower the percentage of affected fruit with calyx alteration symptoms [38, 39]. In fact, 3,5,6-TPA is currently used in the postharvest industry at a dose of 40 ppm and is applied with drenchers [39].

Other plant growth regulators, such as HF-Calibra® (SIPCAM INAGRA, Spain) with active ingredient MCPA-thioethyl (S-Ethyl-4-chloro-o-tolyloxythioacetate), have been tested in the most important Spanish early-season citrus varieties subjected to degreening treatment at different concentrations (10, 20, 40, and 60 ml/L) [26]. That study revealed that this auxin contributes to decreasing calyx senescence triggered by exogenous ethylene. The higher the applied dose, the stronger the effect on preventing calyx abscission.

Another technique to avoid the negative effect of ethylene on calyx senescence is degreening treatments which combine different exposure periods with and without ethylene. This has been evaluated with mandarins and oranges to be exported to the USA from Spain [6, 24]. Optimal degreening process conditions have been established according to both the initial external color and variety [40]. These recommendations are provided in Table 1.

Initial Citrus Color Index (CCI = 1000*a/L*b)EUUSA-Japan
MandarinsOrangesMandarinsOranges
CCI < −13Not recommended
−13 > CCI < −572 h with ethyleneNot recommended48–72 h with ethyleneNot recommended
−5 > CCI < +348 h with ethylene and 72 h without ethylene72 h with ethylene48–72 h without ethylene48–72 h with ethylene
CCI > +324 h with ethylene and 48 h without ethylene48 h with ethylene and 72 h without ethylene24 h without ethylene24 h with ethylene and 48 h without ethylene
CCI > +7Suitable color. Degreening treatment is not necessary

Table 1.

Recommendations for the degreening treatment of Spanish mandarins and oranges to be exported to the EU, USA, or Japan (adapted from Pássaro et al. [40]).

Recently, treatments with Oligochitosan and Chitosan (poly-β-(1,4)-D-glucosamine) have been demonstrated to reduce calyx browning caused by degreening treatment, which has been linked with the inhibition of protopectin, cellulose, and lignin degradation [33].

3.2 Peel disorders

Some citrus cultivars with very thin skin, especially mandarins, can manifest bruising symptoms when they pass along packing lines after being degreened.

This disorder is commonly called ‘zebra skin’ and is caused by mechanical abrasion during the brushing or rolling of fruit in an equatorial area and the cells darken and produce necrotic streaks in the center of fruit segments (Figure 2) [41]. This disorder can also be manifested in non-degreened fruit, but degreening treatment enhances susceptibility to bruising. When degreening treatment is carried out at low humidity, elevated temperature, and high CO2 levels, and for long ethylene exposure times, the susceptibility of fruit showing zebra skin symptoms after packing increases [42]. To avoid this peel alteration, keeping fruit in an ethylene-free atmosphere for at least 12 h after degreening and before packaging, and delaying harvest for 5–7 days after rainy periods, are highly recommended because skin turgidity can increase this damage [43].

Figure 2.

‘Zebra skin’ peel disorder caused by mechanical abrasion in packing line.

Oleocellosis is one of the main postharvest skin disorders to occur in citrus. It is usually caused by mechanical injuries to cells in rind at harvest or on packing lines. Broken cells release the oil, which is phytotoxic to pericarp cells and causes browned areas on affected rind areas. Early-season citrus fruit is more susceptible to oleocellosis [44].

When fruit is subjected to degreening treatment, the mechanical damage caused at harvest and while transporting fruit from fields to packinghouses can lead to olleocelosis. Damaged cells, in which oil extravasation occurs, do not change color during degreening treatment, which leaves green areas on the rind (Figure 3). Moreover, the more turgid rind cells are, the more susceptible fruit are to mechanical damage and they, consequently, show oleocellosis. High environmental humidity, rainy days, or excess irrigation increase fruit peel turgidity, and it is advisable to avoid harvesting after rain or picking fruit early in the morning to avoid dew. Waiting for 24 h from harvesting before handling in containers is also recommended [45]. In addition, cultivar can be a relevant factor since as higher is the density of oil cavities, greater volume, and their position in the pericarp higher is the incidence of the disorder [46].

Figure 3.

Oleocellosis symptoms after degreening treatment.

Another physiological disorder that can be accentuated by postharvest degreening is stem-end rind breakdown (SERB).

SERB symptoms cause the peel tissue around the calyx to collapse, which becomes dark and sunken (Figure 4). SERB is due to excessive water loss and usually appears 2 and 7 storage days after packaging. The fruit that develops this disorder tends to rot more easily. Thinner-skinned fruit grown in humid growing environments, such as Florida, tend to be more prone to SERB than thicker-skinned fruit from arid environments [47]. Including a holding period for 12 to 24 h after degreening treatment and before packing is recommended to avoid SERB. Beneficial effects of ethylene on fruit have been reported; for example, ethylene has been related as a contributor to new wax formation. It also increases the total soft epicuticular wax content in mature citrus fruit, which decreases transpiration, maintains the water balance, and regulates the gas exchange in plants [48].

Figure 4.

Stem-end rind breakdown (SERB) damage.

3.3 Pathological disorders

It has been reported that degreening can aggravate the incidence of some fungi. However, the effect of treatment depends on process conditions. The effect of degreening on Penicillium spp. development depends on the temperature at which treatment takes place. When degreening is performed at 20–22°C (Mediterranean Region conditions), the Penicillium incidence rises because these temperatures are close to optimal for this fungus to develop [21]. Nevertheless, when treatment is carried out at high temperatures (28–29°C) as in Florida, the action of this fungus is inhibited [49]. In this case, treatment can even be seen as curing, which lowers the Penicillium incidence. It has also been reported that Penicillium incidence in degreened fruit is maturation-dependent, and more mature fruit generally show greater severity [50]. After degreening, traditionally the selection of the fruit affected by Penicillium has been manually done, but artificial vision and hyperspectral imaging methods have been recently developed for the early detection of affected fruit [51]. In addition to sorting and discarding affected fruit, the application of washing, sanitation, and specific antifungal treatments before degreening is highly recommended.

Degreening may enhance the anthracnose incidence because ethylene induces conidia germination, appressoria formation, and Colletotrichum gloeosporioides germination due to more accessible nutrients on fruit surfaces [52]. The development of this disease depends on ethylene concentration and treatment duration [53].

Another disease associated with degreening is stem-end rot (SER) caused by Diplodia natalensis. SER develops from latent infections by this fungus established in necrotic fruit button tissue. After harvest, this fungus reactivates and infects fruit through the natural openings that form between fruit and buttons during button separation upon abscission [54]. The SER incidence can be enhanced by degreening treatment when the temperature comes close to 30°C and the ethylene concentration is high [37].

Advertisement

4. Effect of degreening on bioactive compounds

Nowadays, consumers demand fruit with, in addition to an attractive appearance, high sensory and nutritional quality. Citrus fruits are known for their health-promoting benefits due to their high content of bioactive compounds with antioxidant properties. The antioxidant activity of citrus fruit is due to the water-soluble fraction, including vitamin C and polyphenols, and also to the apolar fraction that contains carotenoids. Despite the common dogma that ethylene has a minor effect on the internal ripening processes of citrus fruit, it has not been systematically examined [55].

About the physicochemical parameters of firmness, total soluble solids (TSS), and acidity, there are many reports that ethylene application does not modify them in different citrus cultivars [27, 55, 56, 57]. Nevertheless, the effect of degreening on these attributes can differ depending on the citrus cultivar. In a study that compared three early citrus cultivars, only the ‘Owari’ mandarin had higher softening and higher TSS in degreened fruit (2 ppm, 2–8 days) than in non-degreened ones [58].

In citrus fruit, vitamin C is widely regarded as the most important water-soluble antioxidant compound and an excellent reducing agent [59]. Vitamin C content in Citrus sp. depends on both the maturity stage and other pre- and postharvest factors. Many studies have focused on evaluating the effect of degreening treatment on vitamin C content. Sdiri et al. [6] did not observe any significant reduction in vitamin C in mandarins ‘Clemenules’ and ‘Clemenpons’ after exposing them to ethylene (2 ppm) for 48 h, 72 h, or 120 h. Mayuoni et al. [55] performed a study on different citrus cultivars and found no differences in the vitamin C content of ‘Star Ruby’ grapefruit and ‘Satsuma’ mandarins after degreening treatment lasting up to 72 h. Only ‘Navel’ oranges presented a slight detriment after 72 h, which was attributed to the storage period after the degreening process as no differences were found between degreened and non-degreened fruit. In orange ‘Navelina’ and seven early mandarins (‘Basol’, ‘Clemenrubí’, ‘Clemenpons’, ‘Clemenules’, ‘Orogros’, ‘Oronules’, ‘Prenules’), no differences were observed between the degreened fruit with ethylene (2 ppm, 120 h) and the untreated fruit after cold storage to simulate quarantine conditions (1°C, 16 days), plus a shelf-life period (20°C, 7 days) [24]. In tangerine ‘Batu-55’, a 24-hour degreening treatment at 1, 3, or 5 ppm did not influence vitamin C content [60]. About grapefruit, no differences have been reported in ‘Star Ruby’ between non-degreened and degreened fruit with ethylene (2 ppm, 60 h) after a 21-day storage period at 10°C (to simulate the shipment period) and followed up to 14 days at 20°C (to simulate retail store conditions) [56]. However, in other studies ethylene has been reported to induce an increase in vitamin C. Chaudhary et al. [57] detected more vitamin C in degreened ‘Rio Red’ grapefruit (3.5 ppm ethylene, 72 h) after 35 storage days at 11°C than in non-degreened fruit. Sdiri et al. [61] also observed a slight increase in L-dehydroascorbic acid in degreened ‘Clemenules’ and ‘Clemenpons’ mandarins after simulating a shelf-life period (20°C, 7 days). This increased vitamin C content could be due to the dominant expression of the gene encoding L-galactose-1-phosphatephosphatase (GPP), an enzyme that is related to vitamin C biosynthesis, after finding rising GPP transcript levels in ethylene-treated tomatoes [59].

The exogenous ethylene effect can affect the enzymes involved in plant metabolic pathways, such as phenylalanine ammonia-lyase (PAL), the first enzyme in the phenylpropanoid pathway, or chalcone synthase (CHS) [62]. Regarding phenolic compounds (flavanones, flavones, polymethaoxy flavones, flavanols, hydroxybenzoic acids, and hydroxycinnamic acids), no ethylene effect has been observed in oranges ‘Navel’ and ‘Valencia Delta’, ‘Batu-55’ tangerine and ‘Star Ruby’ grapefruit when submitted to degreening [55, 56, 60, 63]. Sdiri et al. [24] studied the influence of ethylene exposure on the phenolic profile of eight early-season commercial citrus varieties during degreening treatment (2 ppm, 120 h), plus the simulation of quarantine conditions (1°C, 16 days). Only the flavanones profile was modified in the ‘Clemenrubi’ and ‘Clemenpons’ mandarins, whose fruit had been exposed to ethylene and showed the highest total flavanones content after the shelf-life period. An increase in phenolic compounds has also been reported in other studies. Higher total phenolic content has been found in the juice of lemon ‘Fino’ obtained from degreened fruit compared to non-degreened fruit [19]. In ‘Rio Red’ grapefruit, Chaudhary et al. [57] showed that degreened fruit exhibited higher limonin and flavonoids contents and lower furocoumarin levels (mainly 6–7-dihydroxybergamotin) than non-degreened fruit after 7 days of cold storage at 11°C. Nevertheless, in grapefruit ‘Rio Red’, no differences were detected between degreened and non-degreened fruit at the end of the study period (21 days at 11°C, plus 14 days at 21°C). Chaudhary et al. [16] evaluated the effect of ethylene concentration on the flavonoid profile in the same cultivar and found that the 10 ppm-degreened fruit had significantly higher contents for most of the phytochemicals measured compared to the 5 ppm-treated fruit.

Although exposing citrus fruit to ethylene induces carotenoid accumulation in peel [12], scarce information is available about the effect of degreening treatment on the carotenoid content in juice sacs. Matsumoto et al. [17] studied the effect of fruit exposure to different concentrations and temperatures on the carotenoid accumulation in the flavedo and juice vesicles of satsuma mandarins. The results of their study revealed that carotenoid synthesis in citrus was temperature-sensitive, and this effect was tissue-dependent. Storage at 20°C increased carotenoid accumulation in flavedo and maintained carotenoid content in juice sacs. However, storage at 5°C and 30°C slightly increased carotenoid content in flavedo and decreased contents in juice sacs. No exogenous ethylene effect on carotenoid content in the juice sacs of the fruit stored at 20°C and 5°C was observed. Chaudhary et al. [16] also reported that ethylene exposure did not affect the β-carotene and lycopene contents in ‘Star Ruby’ grapefruit juice during degreening treatment.

Therefore, by considering these recent findings, we conclude that degreening treatment can be used to enhance early citrus fruit peel color with minimal effects on nutritional quality.

Advertisement

5. Sensorial quality of degreened citrus fruit

Some studies have pointed out that degreening can impair the taste quality of citrus fruit [55, 64, 65]. Sometimes not using degreening has even been the objective to differentiate citrus fruit by assuming a superior organoleptic quality as in Protected Geographical Indication (PGI) ‘Clémentine de Corse’ [66]. Nevertheless, other studies report that degreening treatments performed under standard conditions do not affect sensory citrus fruit quality [6, 18, 67]. Alteration to the organoleptic quality of degreened fruit has been mainly related to low temperature during their posterior storage period [68].

There are many volatiles responsible for a flavor or aroma sensation in citrus fruit. Moreover, combinations of volatiles yield different flavors than those expected from individual compounds [69]. Citrus fruit presents a complex profile of volatile organic compounds (VOCs), and it is possible to find complex combinations of a subset of up to 300 compounds [70]. Of these, aldehydes and esters are the compounds with the strongest impact on citrus aroma. Changes in the aroma-active compounds of degreened citrus fruit have been reported as being extremely variety-dependent. The changes in the volatile profile of several citrus fruit cultivars submitted to degreening treatment, plus 16-day storage at 1°C and shelf-life, have been studied [71]. While the aroma active compounds of ‘Clemenules’ and ‘Navelina’ are not influenced by ethylene exposure, ‘Oronules’ and ‘Clemenrubí’ presented higher levels of some esters, such as ethyl propionate and ethyl octanoate, in degreened fruit than in non-degreened fruit. Other cultivars, such as ‘Basol’ and ‘Prenules’ mandarins have shown few changes caused by ethylene. It should be noted that despite the effect of degreening on certain volatile compounds in some of these varieties, no differences in sensory quality were observed. Mayuoni et al. [55] detected a minor effect of degreening treatment (4 ppm, 72 h) on volatiles content and composition in the juice of ‘Navel’ oranges, ‘Star Ruby’ grapefruit, and ‘Satsuma’ mandarins. While ethylene exposure did not affect the flavor of oranges and grapefruit, a slight detriment to sensory acceptability was observed in mandarins.

In recent years, several studies have reported no negative degreening effects on sensory citrus fruit properties. In ‘Owari’, ‘Clemenules’ and ‘Oronules’ mandarins and in ‘Navelina’ oranges, Morales et al. [58] have shown that exposure to ethylene (2 ppm for 2–8 days) does not bring about any significant changes in internal sensory characteristics. In fact, consumers were unable to detect the effect of ethylene degreening on physicochemical parameters, although slight differences in soluble solids and acidity were noted in some cultivars. The ethylene degreening treatment has been shown to increase consumer purchase intention. In ‘Fino’ lemons, a sensory analysis determined that degreened fruit subsequently stored for up 28 days at 10°C obtained a similar overall liking to non-degreened fruit. In addition, degreened lemons were perceived as having a better typical lemon aroma than non-degreened lemons [19].

Advertisement

6. Conclusion

We conclude that postharvest degreening treatment is a very useful tool for achieving attractive external citrus fruit color to advance the commercial season without affecting the internal quality, flavor, and nutritional properties of citrus flesh. However, it is necessary to bear in mind that this treatment must be carried out with utmost care to avoid possible physiological disorders on fruit peel. To this end, it is necessary to establish all the process parameters by taking into account the variety to be treated and the optimum harvesting time.

References

  1. 1. Tarancón P, Tárrega A, González M, Besada C. External quality of mandarins: Influence of fruit appearance characteristics on consumer choice. Food. 2021;10(9):2188. DOI: 10.3390/foods10092188
  2. 2. Carmona L, Zacarías L, Rodrigo MJ. Stimulation of coloration and carotenoid biosynthesis during postharvest storage of ‘Navelina’ orange fruit at 12°C. Postharvest Biology and Technology. 2012;74:108-117. DOI: 10.1016/j.postharvbio.2012.06.021
  3. 3. Lafuente MT, Alférez F, Romero P. Postharvest ethylene conditioning as a tool to reduce quality loss of stored mature sweet oranges. Postharvest Biology and Technology. 2014;94:104-111. DOI: 10.1016/j.postharvbio.2014.03.011
  4. 4. Lafuente MT, Sala JM, Zacarias L. Active oxygen detoxifying enzymes and phenylalanine ammonia-lyase in the ethylene-induced chilling tolerance in citrus fruit. Journal of Agricultural and Food Chemistry. 2004;52(11):3606-3611. DOI: 10.1021/jf035185i
  5. 5. González-Candelas L, Alamar S, Sánchez-Torres P, Zacarías L, Marcos JF. A transcriptomic approach highlights induction of secondary metabolism in citrus fruit in response to Penicillium digitatum infection. BMC Plant Biology. 2010;10(194). DOI: 10.1186/1471-2229-10-194
  6. 6. Sdiri S, Navarro P, Monterde A, Benabda J, Salvador A. New degreening treatments to improve the quality of citrus fruit combining different periods with and without ethylene exposure. Postharvest Biology and Technology. 2012;63(1):25-32. DOI: 10.1016/j.postharvbio.2011.08.005
  7. 7. Barry CS, Giovannoni JJ. Ethylene and fruit ripening. Journal of Plant Growth Regulation. 2007;26:143. DOI: 10.1007/s00344-007-9002-y
  8. 8. Eaks IL. Respiratory response, ethylene production, and response to ethylene of citrus fruit during ontogeny. Plant Physiology. 1970;45:334-338
  9. 9. Alós E, Distefano G, Rodrigo MJ, Gentile A, Zacarías L. Altered sensitivity to ethylene in ‘Tardivo’, a late-ripening mutant of Clementine mandarin. Physiologia Plantarum. 2013;147:1300-1315. DOI: 10.1111/ppl.12133
  10. 10. Yin XR, Xie XL, Xia XJ, Yu JQ , Ferguson IB, Giovannoni JJ, et al. Involvement of an ethylene response factor in chlorophyll degradation during citrus fruit degreening. The Plant Journal. 2016;86(5):403-412. DOI: 10.1111/tpj.13178
  11. 11. Fujii H, Shimada T, Sugiyama A, Nishikawa F, Endo T, Nakano M, et al. Profiling ethylene-responsive genes in mature mandarin fruit using a citrus 22 K oligoarray. Plant Science. 2007;173:340-348. DOI: 10.1016/j.plantsci.2007.06.006
  12. 12. Rodrigo MJ, Zacarias L. Effect of postharvest ethylene treatment on carotenoid accumulation and the expression of carotenoid biosynthetic genes in the flavedo of orange (Citrus sinensis L. Osbeck) fruit. Postharvest Biology and Technology. 2007;43(1):14-22. DOI: 10.1016/j.postharvbio.2006.07.008
  13. 13. Purvis AC, Barmore CR. Involvement of ethylene in chlorophyll degradation in peel of citrus fruits. Plant Physiology. 1981;68(4):854-856. DOI: 10.1104/pp.68.4.854
  14. 14. Cuquerella J, Salvador A, Martínez Jávega JM, Navarro P. Effect of quarantine cold treatment on early-season Spanish mandarins. Acta Horticulturae. 2005;682:743-748. DOI: 10.17660/ActaHortic.2005.682.97
  15. 15. Miller WM, Nelson B, Richard R, Ismail MA. Ethylene measurement and control in Florida citrus degreening. In: Integrated View of Fruit & Vegetable Quality. Florida: CRC Press; 2018. pp. 154-162
  16. 16. Chaudhary PR, Bang H, Jayaprakasha GK, Patil BS. Effect of ethylene degreening on flavonoid pathway gene expression and phytochemicals in Rio red grapefruit (Citrus paradisi Macf). Phytochemistry Letters. 2017;22:270-279. DOI: 10.1016/j.phytol.2017.09.016
  17. 17. Matsumoto H, Ikoma Y, Kato M, Nakajima N, Hasegawa Y. Effect of postharvest temperature and ethylene on carotenoid accumulation in the flavedo and juice sacs of Satsuma mandarin (Citrus unshiu Marc.) fruit. Journal of Agricultural and Food Chemistry. 2009;57(11):4724-4732. DOI: 10.1021/jf9005998
  18. 18. Martínez-Jávega JM, Monterde A, Navarro P, Salvador A. Response of new clementines to degreening treatment. Proceedings of the International Society of Citriculture. 2008;11:1342-1346
  19. 19. Serna-Escolano V, Giménez MJ, García-Pastor ME, Dobón-Suárez A, Pardo-Pina S, Zapata PJ. Effects of degreening treatment on quality and shelf-life of organic lemons. Agronomy. 2022;12(2):270. DOI: 10.3390/agronomy12020270
  20. 20. Porat R, Weiss B, Cohen L, Daus A, Goren R, Droby S. Effects of ethylene and 1-methylcyclopropene on the postharvest qualities of ‘Shamouti’ oranges. Postharvest Biology and Technology. 1999;15(2):155-163. DOI: 10.1016/S0925-5214(98)00079-9
  21. 21. Smilanick JL, Mansour MF, Sorenson D. Pre-and postharvest treatments to control green mold of citrus fruit during ethylene degreening. Plant Disease. 2006;90(1):89-96. DOI: 10.1094/PD-90-0089
  22. 22. Goedhals-Gerber LL, Khumalo G. Identifying temperature breaks in the export cold chain of navel oranges: A Western Cape case. Food Control. 2020;110:107013. DOI: 10.1016/j.foodcont.2019.107013
  23. 23. Zhang J, Timmer LW. Preharvest application of fungicides for postharvest disease control on early season tangerine hybrids in Florida. Crop Protection. 2007;26(7):886-893. DOI: 10.1016/j.cropro.2006.08.007
  24. 24. Sdiri S, Navarro P, Monterde A, Benabda J, Salvador A. Effect of postharvest degreening followed by cold-quarantine treatment on vitamin C, phenolic compounds and antioxidant activity of early-season citrus fruit. Postharvest Biology and Technology. 2012;65:13-21. DOI: 10.1016/j.postharvbio.2011.10.010
  25. 25. Van Wyk AA, Huysamer M, Barry GH. Extended low-temperature shipping adversely affects rind colour of ‘Palmer Navel’ sweet orange [Citrus sinensis (L.) Osb.] due to carotenoid degradation but can partially be mitigated by optimising post-shipping holding temperature. Postharvest Biology and Technology. 2009;53:109-116. DOI: 10.1016/j.postharvbio.2009.04.004
  26. 26. Sdiri S, Navarro P, Salvador A. Postharvest application of a new growth regulator reduces calyx alterations of citrus fruit induced by degreening treatment. Postharvest Biology and Technology. 2013;75:68-74. DOI: 10.1016/j.postharvbio.2012.08.004
  27. 27. Ladaniya MS, Singh S. Use of ethylene gas for degreening of sweet orange (Citrus sinenesis Osbeck) cv. Mosambi Journal of Science and Industrial Research. 2001;60:662-667
  28. 28. Cohen E. The effect of temperature and relative humidity during degreening on the coloring of shamouti orange fruit. Journal of Horticultural Science. 1978;53:143-146
  29. 29. Wills RBH, Warton MA, Mussa DMDN, Chew LP. Ripening of climacteric fruits initiated at low ethylene levels. Australian Journal of Experimental Agriculture. 2001;41:89-92. DOI: 10.1071/EA00206
  30. 30. Cronjé PJR, Crouch EM, Huysamer M. Postharvest calyx retention of citrus fruit. International Society of Horticultural Science. 2005;628:369-376
  31. 31. Taylor JE, Whitelaw CA. Signals in abscission. The New Phytologist. 2001;15:323-339
  32. 32. Alhassan N, Golding JB, Wills RBH, Bowyer MC, Pristijono P. Long term exposure to low ethylene and storage temperatures delays calyx senescence and maintains afourer mandarins and navel oranges quality. Food. 2019;8:19
  33. 33. Deng L, Yin B, Yao S, Wang W, Zeng K. Postharvest application of oligochitosan and chitosan reduces calyx alterations of citrus fruit induced by ethephon degreening treatment. Journal of Agricultural and Food Chemistry. 2016;64:7394-7403. DOI: 10.1021/acs.jafc.6b02534
  34. 34. Salvador A, Navarro P, Monterde A, Martínez-Jávega JM. Postharvest application of auxins to control calyx senescence in clementines submitted to degreening treatment. Proceedings of the International Society Citriculture. 2008;11:1377-1382
  35. 35. Carvalho CP, Salvador A, Navarro P, Monterde A, Martinez-Jávega JM. Effect of auxin treatments on calyx senescence in the degreening of four mandarin cultivars. HortScience. 2008;43(3):747-752
  36. 36. Martínez-Jávega JM, Monterde A, Navarro P, Salvador A. Response of new Clementines to degreening treatment. In: Proceedings of Program and Abstracts, 11th International Citrus Congress (ISC Congress); 2008; Wuhan, China, 333.
  37. 37. Brown GE, Burns JK. Enhanced activity of abscission enzymes predisposes oranges to invasion by Diplodia natalensis during ethylene degreening. Postharvest Biology and Technology. 1998;14:217-227
  38. 38. Salvador A, Navarro P, Monterde A, Martínez-Jávega JM. Postharvest application of auxins to control calyx senescence in clementines submitted to degreening treatment. In: Proceedings of the International Society of Citriculture; Spain. 2011. pp. 1377-1382
  39. 39. Tormo DJ, Sdiri S, Conesa E, Navarro P, Salvador A. Application of 3,5,6-TPA under commercial conditions to control calyx senescence associated to degreening treatment. Acta Horticulturae. 2015;1065:1655-1661. DOI: 10.17660/ActaHortic.2015.1065.212
  40. 40. Pássaro C, Navarro P, Salvador A. Poscosecha. In: Garcés L, Corporación Universitaria Lasallista, editors. Cítricos: cultivo, poscosecha e industrialización. 2012. pp. 223-284
  41. 41. Krajewsky AJ. Pittaway. In: Barry GH, editor. Common Defects Associated with Degreening of Citrus. Nelspruit, South Africa: Citrus Research International (Pty) Ltd; 2002
  42. 42. Petracek PD, Kelsey DF, Grierson W. In: Wardowski W, Miller WM, Hall DJ, Grierson W, editors. Physiological Peel Disorders. Fresh Citrus Fruit. 2nd ed. Florida, USA: Florida Science Source, Inc; 2006. pp. 397-442
  43. 43. Albrigo LG. Water relations and citrus fruit quality. In: Sauls JW, Jackson LK, editors. Water Realations. Gainiville: University of Florida Fruit/Crops Department; 1975. pp. 41-48
  44. 44. Zheng Y, He S, Yi S, Zhou Z, Mao S, Zhao X, et al. Characteristics and oleocellosis sensitivity of citrus fruits. Scientia Horticulturae. 2010;123(3):312-317. DOI: 10.1016/j.scienta.2009.09.018
  45. 45. Lafuente MT, Zacarias L. Postharvest physiological disorders in citrus fruit. Ingentaconnect. 2006;9:1-9. DOI: 10.2212/spr.2006.1.2
  46. 46. Montero CRS, Schwarz LL, dos Santos LC, dos Santos RP, Bender RJ. Oleocellosis incidence in citrus fruit in response to mechanical injuries. Scientia Horticulturae. 2012;134:227-231. DOI: 10.1016/j.scienta.2011.10.026
  47. 47. Ritenour MA, Dou H. Stem-End Rind Breakdown of Citrus Fruit: HS936/HS193, 7/2003.EDIS, 2003, 13.
  48. 48. Cajuste JF, González-Candelas L, Veyrat A, García-Breijo FJ, Reig-Armiñana JR, Lafuente M. Epicuticular wax content and morphology as related to ethylene and storage performance of ‘Navelate’ orange fruit. Postharvest Biology and Technology. 2010;55:29-35
  49. 49. Ritenour MA, Miller WM, Wardowski WW. Recommendations for Degreening Florida Fresh Citrus Fruits. Circular 1170. Horticultural Sciences Department. 2003. Florida Cooperative Extension Service, IFAS, University of Florida, Gainesville.
  50. 50. Moscoso-Ramírez PA, Palou L. Effect of ethylene degreening on the development of postharvest penicillium molds and fruit quality of early season citrus fruit. Postharvest Biology and Technology. 2014;91:1-8. DOI: 10.1016/j.postharvbio.2013.12.008
  51. 51. Lorente D, Escandell-Montero P, Cubero S, Gómez-Sanchís J, Blasco J. Visible–NIR reflectance spectroscopy and manifold learning methods applied to the detection of fungal infections on citrus fruit. Journal of Food Engineering. 2015;163:17-24. DOI: 10.1016/j.jfoodeng.2015.04.010
  52. 52. Wild BL. Ethylene gas burn of Washington navel oranges-a form of anthracnose induced by degreening and controlled by brushing or applying fungicides. Australian Journal of Experimental Agriculture. 1990;30(4):565-568. DOI: 10.1071/EA9900565
  53. 53. Tuset JJ, Garcia J, Hinarejos C. Effect of intermittent Degreening Method on Decay of Satsuma Mandarin. In: Goren R, Mendel K, editors. Proceeding of the Sixth International Citrus Congress. 1988. pp. 1461-1465
  54. 54. Zhang J. Lasiodiplodia theobromae in Citrus Fruit (Diplodia Stem-End Rot). In: Bautista-Baños S, editors. Postharvest Decay Control Strategies. Academic Press; 2014. p. 309-335. DOI: 10.1016/B978-0-12-411552-1.00010-7
  55. 55. Mayuoni L, Tietel Z, Patil BS, Porat R. Does ethylene degreening affect internal quality of citrus fruit? Postharvest Biology and Technology. 2011;62:50-58. DOI: 10.1016/j.postharvbio.2011.04.005
  56. 56. Chaudhary P, Jayaprakasha GK, Porat R, Patil BS. Degreening and postharvest storage influences ‘Star Ruby’ grapefruit (Citrus paradisi Macf.) bioactive compounds. Food Chemistry. 2012;135:1667-1675. DOI: 10.1016/j.foodchem.2012.05.095
  57. 57. Chaudhary PR, Jayaprakasha GK, Patil BS. Ethylene degreening modulates health promoting phytochemicals in Rio Red grapefruit. Food Chemistry. 2015;188:77-83. DOI: 10.1016/j.foodchem.2015.04.044
  58. 58. Morales J, Tárrega A, Salvador A, Navarro P, Besada C. Impact of ethylene degreening treatment on sensory properties and consumer response to citrus fruits. Foodservice Research International. 2020;127:108641. DOI: 10.1016/j.foodres.2019.108641
  59. 59. Mditshwa A, Magwaza LS, Tesfay SZ, Opara UL. Postharvest factors affecting vitamin C content of citrus fruits: A review. Scientia Horticulturae. 2017;218:95-104. DOI: 10.1016/j.scienta.2017.02.024
  60. 60. Kailaku SI, Nurjanah R, Jamal IB, Broto W. The effect of degreening on antioxidants of tangerine cv. Batu-55. In: IOP Conference Series: Earth and Environmental Science. Vol. 542. 2020. p. 012018
  61. 61. Sdiri S, Navarro P, Ben Abda J, Monterde A, Salvador A. Antioxidant activity and vitamin C are not affected by degreening treatment of clementine mandarins. Acta Horticulturae. 2012;934:893-899. DOI: 10.17660/ActaHortic.2012.934.119
  62. 62. El-Kereamy A, Chervin C, Roustan JP, Cheynier V, Souquet JM, Moutounet M, et al. Exogenous ethylene stimulates the long-term expression of genes related to anthocyanin biosynthesis in grape berries. Physiologia Plantarum. 2003;119:175-182. DOI: 10.1034/j.1399-3054.2003.00165.x
  63. 63. Pereira GDS, Machado FLDC, Costa J. Quality of ‘Valencia Delta’ orange after degreening and coating with wax. Revista Brasileira de Engenharia Agrícola e Ambiental. 2016;20:936-940. DOI: 10.1590/1807-1929/agriambi.v20n10p936-940
  64. 64. Poole ND, Gray K. Quality in citrus fruit: To degreen or not degreen? British Food Journal. 2002;104:492-505. DOI: 10.1108/00070700210418730
  65. 65. Baldwin EA, Bai J, Plotto A, Ritenour MA. Citrus fruit quality assessment; producer and consumer perspectives. Stewart Postharvest Rev. 2014;10:1-7
  66. 66. Belmin R, Casabianca F, Meynard JM. Contribution of transition theory to the study of geographical indications. Environmental Innovation and Societal Transitions. 2018;27:32-47. DOI: 10.1016/j.eist.2017.10.002
  67. 67. Tietel Z, Weiss B, Lewinsohn E, Fallik E, Porat R. Improving taste and peel color of early-season Satsuma mandarins by combining high-temperature conditioning and degreening treatments. Postharvest Biology and Technology. 2010;57(1):1-5. DOI: 10.1016/j.postharvbio.2010.01.015
  68. 68. Tietel Z, Plotto A, Fallik E, Lewinsohn E, Porat R. Taste and aroma of fresh and stored mandarins. Journal of the Science of Food and Agriculture. 2011;91:14-23. DOI: 10.1002/jsfa. 4146
  69. 69. Chambers E, Koppel K. Associations of volatile compounds with sensory aroma and flavor: The complex nature of flavor. Molecules. 2013;18(5):4887-4905. DOI: 10.3390/molecules18054887
  70. 70. González-Mas MC, Rambla JL, Alamar MC, Gutiérrez A, Granell A. Comparative analysis of the volatile fraction of fruit juice from different Citrus species. PLoS One. 2011;6(7):e22016. DOI: 10.1371/journal.pone.0022016
  71. 71. Sdiri S, Rambla JL, Besada C, Granell A, Salvador A. Changes in the volatile profile of citrus fruit submitted to postharvest degreening treatment. Postharvest Biology and Technology. 2017;133:48-56. DOI: 10.1016/j.postharvbio.2017.07.001

Written By

Julia Morales, Lourdes Cervera, Pilar Navarro and Alejandra Salvador

Submitted: 12 April 2022 Reviewed: 02 May 2022 Published: 04 July 2022