Energy metabolism and fruit quality of Rocha pear as affected by oxygen partial pressures and 1-methylcyclopropene
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1 Energy metabolism and fruit quality of Rocha pear as affected by oxygen partial pressures and 1-methylcyclopropene Adriano Saquet 1,2 & Domingos Almeida 2 1 Instituto Federal de Educação, Ciência e Tecnologia Farroupilha Campus Panambi, Rua Erechim 860, Panambi, RS, Brazil 2 Instituto Superior de Agronomia, Universidade de Lisboa, Tapada da Ajuda, Lisboa, Portugal. address: dalmeida@isa.ulisboa.pt Abstract The effect of low oxygen partial pressures (po2) and 1-methylcyclopropene (1- MCP) on energy metabolism and quality maintenance of Rocha pear was examined. Fruit were stored under: regular air (RA); 3.0 kpa O2; 0.5 kpa O2; or treated with 1-MCP 150 nl L -1 and then stored under 3.0 and 0.5 kpa O2. Fruits were analyzed after 44, 96 and 136 days of storage followed by shelf-life at 20 C. Ethylene production rate was highest in pear stored in RA-storage, followed by those at 3.0 kpa and 0.5 kpa O2. 1-MCP treatment strongly suppressed the ethylene production. The effect of 1-MCP and po2 on respiration rates was similar to that on ethylene production; 1-MCP reduced respiration during 9 days of shelf-life. ATP concentrations, adenylate energy charge (AEC) and the total pool of adenylates were significantly higher in fruit stored in RA than under CA. Fruits kept under 0.5 kpa O2 ripened to a firmness of 17.9 N and skin hue angle of 98.5º after 7 days shelf-life. Titratable acidity and total soluble solids did not change significantly during storage period. In conclusion, fruits stored at low po2 had lower ATP concentrations and lower energy charge than fruit stored in RA-storage. However, the effect of po2 on energy metabolism prevailed over that of 1-MCP treatment. Keywords: adenylate energy charge, controlled atmosphere storage, fruit quality, respiration rate, Pyrus communis L. Introduction Rocha pear can be stored at -1º to 0 ºC in regular air (RA) or controlled atmosphere (CA). This European pear cultivar grown under Portuguese climactic conditions is susceptible to both superficial scald and internal disorders (Silva et al., 2010; Almeida et al., 2016). Pears, in general, do not tolerate the very low oxygen partial pressure (po2) that are used during CA-storage of apples (Streif et al., 2003). Low po2 reduces energy metabolism and results in a low energy status within fruit tissues (Saquet et al., 2000; Veltman et al., 2003). However, responses of Rocha pear to ultra-low po2 are not known. 1-MCP is an effective treatment to prevent superficial scald in Rocha pear (Isidoro and Almeida, 2006; Almeida et al., 2016). However, the recommended concentration of 300 nl L -1 1-MCP can strongly delay post-storage ripening of Rocha pear, leading to a texture perceived as poor and post-storage conditioning is not adequately performed. 1-MCP and low po2 storage are at the present moment, the most reliable technologies to assure long-term storage of Rocha pear with good fruit quality. Therefore, since post-storage ripening of Rocha pear is dependent on 1-MCP dose and doses lower than the recommended can effectively control superficial scald (Isidoro and Almeida, 2006; Almeida et al., 2016) it is necessary to assess the 1-MCP treatment at 150 nl L -1. Actas Portuguesas de Horticultura nº 28 2ª Edição 249
2 The aim of this study was to evaluate the storage ability of Rocha pear under 3.0 and 0.5 kpa O2 combined or not with 1-MCP treatment at half the recommended dose. Emphasis was placed on the effects of storage regimes on physiological changes related to ethylene production, respiration rates and energy, specifically to ATP concentration and adenylate energy charge during the storage period. Material and Methods Plant material and storage conditions. Fruits of pear (Pyrus communis L. Rocha ) were harvested with a starch index of 8.2 (1 to 10 scale), flesh firmness of 52.4 N, total soluble solids (TSS) of 11.2%, titratable acidity of 0.2% expressed on malic acid equivalents, and a skin hue angle of 106.4º. 1-MCP (Agrofresh, Inc., Springhouse, PA, USA) was applied at a dose of 150 nl L -1 for 24 h at 0 ºC. After the treatment with 1-MCP fruits were stored for 32 days in air at -0.5 C, 95% relative humidity (RH) before imposition of controlled atmosphere conditions. 1-MCP-treated and untreated fruits were then stored at -0.5±0.3 C and 95% RH for 136 days in RA or under 3.0 kpa O kpa CO2 or 0.5 kpa O kpa CO2. O2 partial pressures were lowered by flushing N2 and the gas concentrations monitored by gas analyzers (Isolcell Italia, Laives, Italy). Excess CO2 was scrubbed by an automatic system using a 30% KOH-solution. Untreated fruits were stored in RA at the same temperature, RH, and the same CA-conditions used for 1-MCP-treated fruits, but the gas regime was imposed within 24 h of storage. Evaluation of fruit quality attributes. Fruit quality traits were analyzed immediately after 44, 96 and 136 days in storage and following a 7-days shelf-life period at 20 ºC after each storage period. Surface color was measured in CIE L*a*b* color space with a tri-stimulus CR- 400 Chroma Meter (Konica Minolta, Tokyo, Japan). Measurements were made in the widest part of the fruit in three replicate of 5 fruits each. Flesh firmness was measured after peel removal with a penetrometer (T.R. Turoni, Forli, Italy) equipped with an 8 mm probe. Firmness was measured twice in each fruit, in pared sides, in three replicated batches of 5 fruits each. Fruits were cut in the equatorial region and 10 mm thick disk excised and used for juice extraction. TSS were measured in the juice with a digital refractometer (Hanna Instruments, Woonsocket, USA). An aliquot of 10 ml juice was diluted in 90 ml distilled water and the solutions titrated with 0.1 M NaOH until ph 8.1. Titratable acidity was expressed as malic acid equivalents. Ethylene and respiration measurements. Samples of 4 fruits, in 3 replicates, were placed inside of 2.15 L sealed glass jars. After a 2 h incubation, the headspace was sampled for ethylene analysis by gas chromatograph (Trace 1300, Thermo Fisher Scientific Inc., Marietta, USA) with a flame ionization detector and a capillary glass column. The CO2 release was measured in the same fruit samples, which were used for ethylene measurements. An Oxycarb 6 gas analyzer (Isolcell Italia, Laives, Italy) with an infrared sensor was used for analysis. The CO2 release was measured by a continuous flow at a rate of 100 ml min -1. Ethylene production and the CO2 release of pear fruits were measured during 9 days of fruit exposure to air at 20 C. Measurement of adenylate nucleotides and AEC calculation. The concentration of adenylate nucleotides were measured at the fruit core. Cylinders were Actas Portuguesas de Horticultura nº 28 2ª Edição 250
3 excised from the core region of the fruit and seeds carefully removed. After removal, cylinders were frozen in liquid nitrogen and freeze-dried at -50 C and -100 kpa. Samples were powdered and used for extraction and assessments according to Saquet et al. (2003) with minor adaptations. AEC was calculated according to Atkinson and Walton (1967). Results and discussion Quality attributes. Changes in fruit firmness after 136 days storage of Rocha pear are shown in Figure 1 A. Firmness retention was higher in pears stored under low po2 and low po2 combined with 1-MCP treatment. After 136 days of storage RA-stored pear fruits were not marketable due to the very low firmness after the 7 days shelf-life at 20 C. The storage of pear under 3 kpa O2 maintained a higher firmness than RA-stored fruits, but only during storage. Following 7 days of shelf-life at 20 ºC, fruits stored under 3 kpa O2 had the same firmness of RA-stored fruits. The combination of 1-MCP and 32 days delayed CA with storage at 3.0 or 0.5 kpa O2 maintained higher firmness in Rocha pear, including after the shelf-life period. Fruits of RA-storage were significant yellower than the other treatments (Figure 1 B), even after the shelf-life period. Green color retention was higher in fruit treated 1- MCP and stored under 0.5 kpa O2. This effect of CA-storage and 1-MCP on green color maintenance in pear is well documented (Rizzolo et al., 2015; Vanoli et al., 2016). Titratable acidity and total soluble solids of Rocha pear (Figure 1 C and D, respectively) did not change significantly after 136 days of storage, with the exception of RA-stored fruit in which acidity decreased. Ethylene production and respiration rates. Ethylene production in Rocha pear is shown in Figure 2 A. The post-storage residual effect of CA conditions and 1- MCP treatment remained intense during shelf-life, and stronger in 1-MCP-treated fruits. RA-stored pears advanced ripening leading to a lower rate of ethylene production than fruits under 0.5 kpa O2. Fruit treated with 150 nl L -1 1-MCP and stored under 0.5 kpa O2 failed to recover the ethylene emission after storage; ethylene production rate in these fruits remained at 3.1 µl L -1 even after 9 days of shelf-life. This strong inhibitory effect of 1-MCP on ethylene production in Rocha pear confirms the effectiveness of ethylene blockage also reported in Conference (de Wild et al., 1999), Abbé Fétel (Rizzolo et al., 2015) and Bartlett (Argenta et al., 2016) pears. Respiration of Rocha pear is presented in Figure 2 B. Fruit respiration during shelf-life after 136 days of storage did not match ethylene production. Even after storage under 0.5 kpa O2 the respiration of Rocha pear increased normally at same intensity fruit stored in RA and 3 kpa O2. 1-MCP treatment reduced post-storage respiration rate, which nonetheless increased during shelf-life. 1-MCP treatment in pears have shown marked inhibiting effects on respiration of d Anjou (Argenta et al., 2003), La France (Kubo et al., 2003) and Bartlett (Argenta et al., 2016) pears. The weaker residual effect of CA-storage on the respiration rate of Rocha pear maybe related to the sensitivity of Rocha pear to ethylene; even at lower ethylene production rates, the respiration increased in air at 20 C. The inhibitory effect of CA on post-storage ripening is reported in apples (Brackmann et al., 1993), but Rocha pear has a ripening capacity after longterm CA-storage (Silva et al., 2010; Almeida et al., 2016). Changes in ATP and AEC. ATP concentrations remained higher in Rocha pear stored in RA than in CA-storage conditions (Figure 3 A). 1-MCP treatment had a smaller effect on ATP concentration than the oxygen partial pressures. Very similar behavior was observed in Conference pear (Saquet et al., 2003) and Jonagold apple (Xuan and Streif, 2008). Jonagold apple treated with 1-MCP at 625 nl L -1 had lower ATP concentrations during shelf-life after 8.5 months in CA-storage (Xuan and Streif, 2008). Actas Portuguesas de Horticultura nº 28 2ª Edição 251
4 The changes in AEC during storage of Rocha pear was similar to those observed in ATP concentrations (Figure 3 B). The energy metabolism, mainly regarding the ATP concentrations and AEC, has been considered an important and possible factor that can be involved in the development of internal disorders in apples and pears during long-term CA-storage (Saquet, et al., 2000, 2003, Veltman et al. 2003). Conclusions 1-MCP at 150 µl L -1 reduced ethylene production and respiration rates further than the effect of low po2 alone. Fruits stored at low po2 had lower ATP concentrations and lower energy charge than fruit stored in RA-storage. However, the effect of po2 on energy metabolism prevailed over that of 1-MCP treatment. References Almeida, D.P.F., Carvalho, R. & Dupille, E Efficacy of 1-methylcyclopropene on the mitigation of storage disorders of Rocha pear under normal refrigerated and controlled atmospheres. Food Science and Technology International 22, 5: Argenta, L.C., Fan, X. & Matheis, J.P Influence of 1-Methylcyclopropene on ripening, storage life, and volatile production by d Anjou cv. pear fruit. Journal of Food Chemistry 51(13): Argenta, L.C., Mattheis, J.P. & Fan, X.; Amarante, C.V.T Managing Bartlett pear fruit ripening with 1-methylcyclopropene reapplication during cold storage. Postharvest Biology and Technology 113: Atkinson, D.E. & Walton, G.M Adenosine triphosphate conservation in metabolic regulation. Rat liver citrate cleavage enzyme. Journal of Biological Chemistry 242: Brackmann, A., Streif, J. & Bangerth, F Relationship between a reduced aroma production and lipid metabolism of apples after long-term controlled-atmosphere storage. Journal of the American Society for Horticultural Science 118(2): De Wild, H.P.J., Woltering, E.J. & Peppelenbos, H.W Carbon dioxide and 1-MCP inhibit ethylene production and respiration of pear fruit by different mechanisms. Journal of Experimental Botany 50(335): Isidoro, N. & Almeida, D.P.F α-farnesene, conjugated trienols, and superficial scald in Rocha pear as affected by 1-methylcyclopropene and diphenylamine. Postharvest Biology and Technology 42: Kubo, Y., Hiwasa, K., Owino, W.O., Nakano, R. & Inaba, A Influence of time and concentration of 1-MCP application on the shelf life of La France fruit. HortScience 38(17): Rizzolo, A., Grassi, M. & Vanoli, M Influence of storage (time, temperature, atmosphere) on ripening, ethylene production and texture of 1-MCP treated Abbé Fétel pears. Postharvest Biology and Technology 109: Saquet, A.A., Streif, J. & Bangerth, F Changes in ATP, ADP and pyridine nucleotide levels related to the incidence of physiological disorders in Conference pears and Jonagold apples during controlled atmosphere storage. Journal of Horticultural Science and Biotechnology 75: Saquet, A.A., Streif, J. & Bangerth, F Energy metabolism and membrane lipid alterations in relation to brown heart development in Conference pears during delayed controlled atmosphere storage. Postharvest Biology and Technology 30: Actas Portuguesas de Horticultura nº 28 2ª Edição 252
5 Silva, F.P., Gomes, M.H., Fidalgo, F., Rodrigues, J.A. & Almeida, D.P.F Antioxidant properties and fruit quality during long-term storage of Rocha pear: Effects of maturity and storage conditions. Journal of Food Quality 33: Streif, J., Saquet, A.A. & Xuan, H CA-related disorders of apples and pears. Acta Horticulturae 600: Vanoli, M., Grassi, M. & Rizzolo, A Ripening behavior and physiological disorders of Abate Fetel pears treated at harvest with 1-MCP and stored at different temperatures and atmospheres. Postharvest Biology and Technology 111: Veltman, R.H., Lenthéric, I., van der Plas, L.H.W. & Peppelenbos, H Internal browning in pear fruit (Pyrus communis L. cv. Conference) may be a result of a limited availability of energy and antioxidants. Postharvest Biology and Technology 28: Xuan, H. & Streif, J Effect of 1-MCP on respiration and concentration of ATP/ADP in the fruit tissue of Jonagold apple after storage. Acta Horticulturae 796: Tables and Figures Figure 1. Flesh firmness (A), skin color (B), acidity (C) and total soluble solids (D) after 136 days in storage at -0.5 ºC and following 7 days shelf-life at 20 C. Vertical bars are standard deviation. Actas Portuguesas de Horticultura nº 28 2ª Edição 253
6 Figure 2. Ethylene production rate (A) and respiration rate (B) of Rocha pear during 9 days shelf-life at 20 C after 136 days in storage. Vertical bars are standard deviation. Figure 3. Changes in ATP (A) and adenylate energy charge (B) during storage of Rocha pear. Vertical bars are standard deviation. Actas Portuguesas de Horticultura nº 28 2ª Edição 254
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