Print version ISSN 0100-204X
Pesq. agropec. bras. vol.46 no.12 Brasília Dec. 2011
'Royal Gala' apple quality stored under ultralow oxygen concentration and low temperature conditions
Qualidade de maçã 'Royal Gala' armazenada em condições de concentração ultrabaixa de oxigênio e baixa temperatura
Anderson Weber; Auri Brackmann; Rogério de Olivera Anese; Vanderlei Both; Elizandra Pivotto Pavanello
Universidade Federal de Santa Maria, Departamento de Fitotecnia, Prédio 77, Cidade Universitária, Bairro Camobi, CEP 97105-900 Santa Maria, RS, Brazil. E-mail: firstname.lastname@example.org, email@example.com, firstname.lastname@example.org, email@example.com, firstname.lastname@example.org
The objective of this work was to evaluate the interaction of ultralow oxygen concentrations (ULO) with storage temperatures and carbon dioxide partial pressures and its influence on fruit quality preservation and on the occurrence of physiological disorders in 'Royal Gala' apples. The experiment was carried out in a completely randomized design, with four replicates 25-fruit. ULO conditions (1.0 kPa O2 + 2.0 kPa CO2; 0.8 kPa O2 + 1.5 kPa CO2; 0.8 kPa O2 + 1.0 kPa CO2; 0.6 kPa O2 + 1.5 kPa CO2; and 0.6 kPa O2 + 1.0 kPa CO2) were tested at 0, 0.5 and 1.0°C, in a 5x3 factorial arrangement. Fruit quality and ripening analyses were performed after eight-month storage plus seven days of shelf-life at 20°C. Oxygen partial pressures below 0.8 kPa increased the occurrence of internal breakdown and mealiness. The best ULO condition was 1.0 kPa O2 + plus 2.0 kPa CO2 at 1.0°C. The interaction of ULO conditions and storage temperatures shows the need of increasing O2 partial pressure at higher storage temperatures.
Key words: Malus domestica, carbon dioxide, controlled atmosphere, decay, physiological disorders.
O objetivo deste trabalho foi avaliar a interação de concentrações ultrabaixas de oxigênio (ULO) com diferentes temperaturas e pressões parciais de gás carbônico sobre a conservação da qualidade e a ocorrência de distúrbios fisiológicos em maçãs 'Royal Gala'. O experimento foi realizado em delineamento inteiramente casualizado, com quatro repetições de 25 frutos. As concentrações ULO (1,0 kPa O2 + 2,0 kPa CO2, 0,8 kPa O2 + 1,5 kPa CO2, 0,8 kPa O2 + 1,0 kPa CO2, 0,6 kPa O2 + 1,5 kPa CO2 e 0,6 kPa O2 + 1,0 kPa CO2) foram avaliadas a 0,0, 0,5 e 1,0°C, em arranjo fatorial de 5x3. As análises da qualidade e amadurecimento dos frutos foram realizadas após oito meses de armazenamento e mais sete dias de exposição a 20°C. As pressões parciais de O2 abaixo de 0,8 kPa aumentaram a ocorrência de degenerescência de polpa e polpa farinácea. A melhor condição de ULO foi a de 1,0 kPa O2 + 2,0 kPa CO2 a 1,0°C. A interação entre condições de ULO e temperaturas de armazenamento evidencia necessidade de aumento das pressões parciais de O2 quando a temperatura de armazenamento é mais elevada.
Palavras-chave: Malus domestica, gás carbônico, atmosfera controlada, podridões, distúrbios fisiológicos.
Controlled-atmosphere storage extend the postharvest life of apple fruit. The system combines low temperatures with low partial pressures of O2 and high partial pressure of CO2, which reduce respiration rates, ethylene (C2H4) biosynthesis and action (Yang & Hoffman, 1984), thereby maintaining the physical and chemical properties of fruit. However, there are still significant postharvest losses of fruit due to pathogens and physiological disorders, which may reach up to 60% depending on the year (Brackmann et al., 2002). Therefore, it has become necessary to improve the currently used storage techniques to reduce fruit loss.
Partial pressures of O2 and CO2 recommended for the storage of 'Royal Gala' apples in Brazil are 1.0 and 2.5 kPa, respectively (Brackmann et al., 2008). It is well documented that low levels of O2 in controlled-atmosphere storage reduce fruit respiration and ethylene production and action. Generally, the lower the metabolic rates, the longer the postharvest life and quality of apples. Therefore, studies have been conducted to define the use of ultralow oxygen partial pressures (Zanella, 2003), to suppress fruit metabolism, and to obtain higher fruit quality by reducing losses.
Under controlled-atmosphere storage, the oxygen partial pressure cannot fall below the minimum limit needed for aerobic energy production. Below this minimum limit, also known as the anaerobic compensation point, the anaerobic respiration becomes the major energy production pathway (Saquet & Streif, 2008). This change in metabolism may cause the accumulation of volatile substances, like ethanol and acetaldehyde, and may ultimately result in the development of physiological disorders such as flesh breakdown (Pedreschi et al., 2009). The lowest oxygen limit may vary among fruit of the same species (Prange et al., 2003), depending on the region, the year of production (Delong et al., 2004), and on the storage temperature (Wright et al., 2010). Therefore, ultralow oxygen must be studied before it is applied commercially for 'Royal Gala' apples.
The lower oxygen limits recommended for the 'Delicious', 'Law Rome' and 'McIntosh' apples are 0.7 kPa, 0.9 kPa and 1.9 kPa, respectively (Gran & Beaudry, 1993). 'Granny Smith' apples stored under O2 partial pressures of 0.7 kPa, from four to six months, showed a ground color identical to the one they had at harvest time, according to Zanella (2003), who also reported a lower occurrence of flesh breakdown, better retention of flesh firmness and total absence of scald in apples stored under ultralow oxygen conditions. For apples cultivated in Brazil, Brackmann et al. (2000) reported that the optimum storage conditions for 'Gala' apples were 0.75 to 1.0 kPaO2, at 1.0°C. However, Ceretta et al. (2010) reported, for the same cultivar stored at 0°C and ≤0.8 kPa O2 conditions, an increase of skin cracking occurrences, internal breakdown and decay compared to fruit stored under 1.0 kPa O2. Discrepancy between these reports is probably due to the distinct temperatures employed in each study, which shows that there might be a relationship between storage temperature and O2 levels in the prolonged maintenance of apple quality.
The objective of this work was to evaluate the interaction of ultralow oxygen partial pressure with different temperatures and carbon dioxide partial pressures and its influence on fruit quality preservation and on the occurrence of physiological disorders in 'Royal Gala' apples.
Materials and Methods
The experiment was carried out at the Núcleo de Pesquisa em Pós-colheita, Departamento de Fitotecnia, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil, in 2008. Fruit samples were harvested in a commercial orchard, in Vacaria county, RS, Brazil. At harvest, fruit showed 6.70 starch index (scale 0, minimum; 10, maximum starch hydrolysis), 92.8 N flesh firmness, and 21.8 ηL g-1 h-1 C2H4 1-aminocyclopropane-1-carboxylic acid (ACC) oxidase activity, and produced 1.33 µL kg-1 h-1 C2H4 and 6.86 mL kg-1 h-1 CO2 (respiration rate).
The experiment was conducted in a completely randomized design, with four replicates of 25 fruit. Five ultralow oxygen conditions were tested at three different temperatures, in a factorial arrangement (5x3). The controlled-atmosphere storage conditions were: 1.0 kPa O2 + 2.0 kPa CO2; 0.8 kPa O2 + 1.5 kPa CO2; 0.8 kPa O2 + 1.0 kPa CO2; 0.6 kPa O2 + 1.5 kPa CO2; and 0.6 kPa O2 + 1.0 kPa CO2. All these conditions were tested at 0, 0.5 and 1.0°C.
The fruit were stored in hermetically sealed experimental chambers with 0.232 m3, which were placed inside a cold storage room with 48 m3 each, at 0, 0.5 and 1.0°C (oscillation of ±0.1°C). The relative humidity inside the chambers was maintained at 96±1%. Temperature was controlled by thermostats and checked daily by bulb mercury thermometers with a 0.1°C resolution inserted in the fruit flesh. The dilution of O2 in the storage chamber was done with injections of N2 obtained from a pressure swing adsorption (PSA) nitrogen generator (Janus & Pergher, Porto Alegre, RS, Brazil). Partial pressures of CO2 were obtained by gas injection from a high pressure cylinder. The desired partial pressures were maintained by automatic gas control equipment (Kronenberger/Climasul, Caxias do Sul, RS, Brazil). The O2 consumed by respiration was replaced by injections of atmospheric air into the chambers, and excessive CO2 produced by respiration was absorbed by a 40% potassium hydroxide solution.
Fruit quality and ripening parameters were evaluated after eight-month storage, plus seven days of shelf-life at 20°C, except for respiration, which was assessed at the removal from the storage chambers and after the six days of air-exposure at 20°C. The parameters decay occurrence, flesh firmness, mealiness, internal breakdown, ACC oxidase activity, ethylene production rate and respiration rate were assessed and detailed as follows.
Decay occurrence was evaluated by counting fruit showing typical fungal lesions larger than 5 mm in diameter.
Flesh firmness was determined with a penetrometer model FT 327 (Effegi Systems, Milan, Italy), equipped with a 11 mm probe and measured in both sides of fruit equatorial region, from which the skin had been previously removed.
Mealiness was determined by visual quantification of fruit exhibiting symptoms related to this physiological disorder (dry and non-juicy flesh).
Internal breakdown was measured by visual evaluation of flesh browning, after transversal cuts across fruit.
ACC oxidase activity was determined in 3 g skin samples extracted from fruit equatorial region, from each experimental unit; these samples were immediately dipped into a solution containing 0.1 mol L-1 ACC and 10 mmol L-1 MES buffer [2-(N-morpholino) ethanesulfonic acid] at pH 6.0; after 30 min, samples were transferred to hermetic 50 mL syringes, to which 1 mL CO2 was added. The ethylene concentration in the syringes was measured by gas chromatography after 30 min, and the results were expressed as ηL g-1 h-1 C2H4 (Bufler, 1986). To analyze ethylene concentration, two gas samples of 1 mL extracted from the headspace of each syringes were injected in a gas cromatograph, Varian Gas Cromatograph Star CX 3400 model, (Varian, Palo Alto, CA, USA), equipped with a flame ionization detector (FID) and a Porapak N80/100 steel column. The column, injector and detector temperatures were 90, 140 and 200°C, respectively.
Ethylene production rate was determined by the use of approximately 1,200 g fruit which were placed into containers with 5,000 mL volume. These containers were hermetically sealed for approximately two hours. Ethylene synthesis, expressed as µL kg-1 h-1 C2H4, measured by gas chromatography, was calculated by taking into account the ethylene concentration, the mass of fruit, the free space inside the container, and time.
Respiration rate was determined by the volume of CO2 production. The air from the same container, used to determine the production of ethylene, was circulated through an electronic CO2 analyzer, with the infrared gas analyzer (IRGA) system (Agri-datalog, Lana, BZ, Italy). Based on CO2 concentration, free space inside the container, fruit weight and closure time, the respiration rate was calculated and expressed as mL kg-1 h-1 CO2.
Before the analysis of variance, the results were tested for normality and homogeneity of errors by the Lilliefors and Bartlett tests, respectively. The parameters that fell outside the normality of errors were transformed by the formula arc sen square root (x + 0.5)/100, while the parameters with heteroscedasticity errors were transformed by the formula log10(x + 1.0) to be returned to the group and then submitted to ANOVA tests. Average values were compared by Tukey's test, at 5% probability.
Results and Discussion
Fruit stored under 0.8 kPa O2 + 1.5 kPa CO2 conditions and exposed for seven days at 20°C showed the lowest occurrence of decay, independently of the storage temperature (Table1). Low O2 partial pressures during the storage reduced the occurrence of decay during the post-storage period, possibly due to the fungistatic effect of low O2 concentration (Neuwald, 2004). Cellular energy production was likely induced by anaerobic respiration under 0.6 kPa O2. As a result, cells were damaged, probably due to accumulation of fermentation products, and became sensitive to infections (Kader, 2002). Ceretta et al. (2010) also reported a higher decay occurrence in 'Gala' apples stored at O2 partial pressures below 0.8 kPa. This partial pressure of O2 (0.8 kPa) also increased decay susceptibility in 'Fuji' apples (Brackmann et al., 2001).
Flesh firmness was not significantly affected by the different ultralow oxygen and CO2 conditions (Table1). Storage temperatures of 0.5 and 1.0°C kept higher flesh firmness, in comparison to 0°C. Brackmann et al. (2008) reported that 'Royal Gala' and 'Galaxy' apples showed greater flesh firmness at 0.5ºC in comparison to -0.5ºC. The loss of flesh firmness is usually linked to rates of respiration and ethylene production (Hiwasa, et al., 2003). In the present study, it was observed that after a six-day exposure to air at 20°C, fruit stored at 0°C showed higher rates of respiration and ethylene production than fruit stored at 0.5 and 1.0°C (Table 2). It has been reported that increased ethylene synthesis induces the expression and the activity of cell-wall degrading enzymes (Prasanna et al., 2007) resulting in loss of firmness.
The occurrence of mealiness had no interaction with ultralow oxygen conditions and temperatures (Table1). There was a lower occurrence of this disorder at 1.0°C storage temperature. However, the storage of apples at 0.8 kPa O2 with 2.0 or 1.5 kPa CO2 resulted in a higher occurrence of mealiness. This physiological disorder is associated with ripening, when protopectin degradation is enhanced (Prasanna et al., 2007), reducing the cell-to-cell adhesion and, ultimately, leading to the development of a mealy aspect. The activity of cell-wall degrading enzymes is highly correlated with ethylene biosynthesis and respiration rate (Wei et al., 2010).
There was a significant interaction between storage temperatures and ultralow oxygen conditions for flesh breakdown (Table 1). The temperature increase from 0 to 1.0°C decreased the occurrence of this disorder, especially in higher O2 partial pressure. According to Streif et al. (2003), many postharvest factors affect the occurrence of flesh breakdown in apples, such as harvest date, time between harvest and cooling, CO2 and O2 partial pressures, and storage interval and storage temperature. Flesh breakdown occurrence was lower at 1.0°C with the highest O2 levels (0.8 and 1.0 kPa O2 associated with 2.0 kPa CO2). However, no statistic difference in the treatment 0.8 kPa O2 + 1.5 kPa CO2 was observed. At 0°C there was a lower occurrence of the disorder in conditions with a lower O2 level of (0.6 kPa O2 + 1.0 kPa CO2), although not differing from the conditions with 0.6 and 0.8 kPa O2 associated to 1.5 kPa CO2. The interaction between temperature and oxygen partial pressure resulted in the need to increasing O2 partial pressures as temperature was increased from 0 to 1.0°C. A possible explanation to this result would be that the solubility of O2 inside the apple flesh decreases as the temperature rises (Yearsley et al., 1997). Consequently, if a lower solubility limits the O2 availability, it is expected that the minimum oxygen limit increases as a function of storage temperature rise. Similar results were reported by Wright et al. (2010) for 'Honeycrisp' apple. Thus, a higher occurrence of this disorder occurs probably due to a higher anaerobic respiration observed in fruit submitted to lower O2 partial pressure. The final products of this reaction, namely ethanol and acetaldehyde, and the imbalance between oxidative and reductive processes cause an energetic collapse and loss of membrane integrity, resulting in flesh breakdown (Franck et al., 2007).
As to ACC oxidase activity, partial pressures of O2 and CO2 showed contrasting effects at different storage temperatures (Table 2). At 0°C, the storage of fruit at 0.6 kPa O2 + 1.5 kPa CO2 resulted in a reduction in ACC activity, although not differing from the conditions with 0.6 kPa O2 + 1.0 kPa CO2. At 0.5°C, however, the controlled-atmosphere storage with 0.6 kPa O2 + 1.5 kPa CO2 caused an increasing effect by inhibiting the ACC oxidase activity, but a difference with 0.8 kPa O2 + 1.5 or 2.0 kPa CO2 condition was not observed. Thus, when storage temperature was 0.5ºC, a higher O2 partial pressure (0.8 kPa) was required to supply the enzyme activity, due to the lower O2 solubility at higher temperatures (Yearsley et al., 1997). Comparing the temperatures, under conditions where O2 partial pressure were maintained at 0.8 or 1.0 kPa, associated to 2.0 kPa CO2, the lowest ACC oxidase activity was measured in fruit stored at 1.0°C. The ACC oxidase, ethylene production rate and flesh breakdown results, showed that, when the storage temperature is increased from 0 to 1.0°C, the O2 partial pressures must also be raised.
Fruit exposed to 0.6 kPa O2, with the two partial pressures of CO2 (1.0 and 1.5 kPa) and 0.8 kPa O2 + 1.5 kPa CO2 at 0°C, showed the lowest ethylene production (Table 2). Comparing the tested temperatures to 0°C, there was a lower ethylene production at 0.5 and 1.0°C, for conditions of 0.8 and 1.0 kPa O2 combined with 2.0 kPa CO2. Lower ethylene production was a result of the lower ACC oxidase activity visible in fruit at high temperature. These results may appear incompatible, but excessive reduction of temperature can cause cell damage and a concomitant increase in ethylene production (Knee et al., 1983) resulting in low fruit quality. In agreement with that, the lower occurrence of physiological disorder was observed in fruit stored at 1.0°C (Table 1).
By the analysis performed soon after removing fruit from the storage chamber, respiration rate was lower in fruit stored under conditions of higher CO2 partial pressure (1.5 and 2.0 kPa) at 0°C (Table 2). However, at 0.5°C, only fruit stored at 0.6 kPa O2 + 1.5 kPa CO2 showed lower respiration rate. After a six-day exposure to air at 20°C, there was no interaction between temperature and controlled-atmosphere storage conditions. Fruit stored at 0.5 and 1.0°C showed lower respiration rate than those kept at 0ºC. It has been reported that 'Royal Gala' and 'Galaxy' apples stored in controlled-atmosphere storage exhibited lower respiration at 0.5°C in comparison to -0.5°C (Brackmann et al., 2008), thus showing an inverted relationship between temperature (in the range of 0 to 1.0°C) and respiration rate.
1. The storage of 'Royal Gala' apples under ultralow oxygen (below 0.8 kPa of O2) conditions reduces the post-storage quality and increases the occurrence of physiological disorders in fruit.
2. The 1ºC storage temperature can keep the quality of 'Royal Gala' apples after eight months of controlled-atmosphere storage.
3. The best ultralow oxygen condition for the storage of 'Royal Gala' apples is 1.0 kPa O2 combined with 2.0 kPa of CO2 at 1.0°C.
4. The O2 partial pressures must be increased when storage temperature is higher.
To Conselho Nacional de Desenvolvimento Cientí-fico e Tecnológico, Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul, for financial support.
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Received on August 1st, 2011 and accepted on November 7, 2011
No artigo "WEBER, A.; BRACKMANN, A.; ANESE, R. de O.; BOTH, V.; PAVANELLO, E.P. 'Royal Gala' apple quality stored under ultralow oxygen concentration and low temperature conditions. Pesquisa Agropecuária Brasileira, v.46, n.12, p.1597-1602, dez. 2011", substituir o conteúdo da Tabela 1 pelo seguinte:
No artigo "MARIGUELE, K.H.; RESENDE, M.D.V. de; VIANA, J.M.S.; SILVA, F.F. e; SILVA, P.S.L. de; KNOP, F. de C. Métodos de análise de dados longitudinais para o melhoramento genético de pinha. Pesquisa Agropecuária Brasileira, v.46, n.12, p.1657-1664, dez. 2011", substituir o conteúdo da Tabela 2 pelo seguinte:
In the paper "WEBER, A.; BRACKMANN, A.; ANESE, R. de O.; BOTH, V.; PAVANELLO, E.P. 'Royal Gala' apple quality stored under ultralow oxygen concentration and low temperature conditions. Pesquisa Agropecuária Brasileira, v.46, n.12, p.1597-1602, Dez. 2011", replace the content of Table 1 by the following:
In the paper "MARIGUELE, K.H.; RESENDE, M.D.V. de; VIANA, J.M.S.; SILVA, F.F. e; SILVA, P.S.L. de; KNOP, F. de C. Métodos de análise de dados longitudinais para o melhoramento genético de pinha. Pesquisa Agropecuária Brasileira, v.46, n.12, p.1657-1664, Dez. 2011", replace the content of Table 2 by the following: