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Metabolic changes in 1-methylcyclopropene (1-MCP)-treated ‘Empire’ apple fruit during storage

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Abstract

‘Empire’ apple fruit are more susceptible to flesh browning at 3.3°C if treated with 1-methylcyclopropene (1-MCP), an inhibitor of ethylene perception. To better understand the metabolic changes associated with this browning, untargeted metabolic profiling with partial least squares analysis has been used to visualize changes in metabolic profile during hypoxic controlled atmosphere (CA) storage, ethylene insensitivity, and disorder development. Overall, most carbohydrates and organic acids were not appreciably affected, but the levels of amino acids and volatile metabolites were significantly affected, by 1-MCP treatment. Sorbitol and levels of some amino acids were elevated towards the end of storage in 1-MCP treated fruit. CA storage reduced the levels of many volatile components and 1-MCP reduced these levels further. Additionally multiple metabolites were associated with the development of flesh browning symptoms. Unlike other volatile compounds, methanol levels gradually increased with storage duration, regardless of 1-MCP treatment, while 1-MCP decreased ethanol production. Results reveal metabolic changes during storage that may be associated with development of flesh browning symptoms.

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References

  • Ackermann, J., Fischer, M., & Amado, R. (1992). Changes in sugars, acids, and amino acids during ripening and storage of apples (cv. Glockenapfel). Journal of Agricultural and Food Chemistry, 40, 1131–1134.

    Article  CAS  Google Scholar 

  • Argenta, L., Fan, X., & Mattheis, J. (2000). Delaying establishment of controlled atmosphere or CO2 exposure reduces ‘Fuji’ apple CO2 injury without excessive fruit quality loss. Postharvest Biology and Technology, 20, 221–229.

    Article  CAS  Google Scholar 

  • Argenta, L. C., Fan, X., & Mattheis, J. P. (2002). Responses of ‘Fuji’ apples to short and long duration exposure to elevated CO2 concentration. Postharvest Biology and Technology, 24, 13–24.

    Article  CAS  Google Scholar 

  • Argenta, L. C., Fan, X., & Mattheis, J. P. (2007). Responses of ‘Golden Delicious’ apples to 1-MCP applied in air or water. HortScience, 42, 1651–1655.

    CAS  Google Scholar 

  • Argenta, L. C., Mattheis, J. P., Fan, X., & Finger, F. L. (2004). Production of volatile compounds by Fuji apples following exposure to high CO2 or low O2. Journal of Agricultural and Food Chemistry, 52, 5957–5963.

    Article  PubMed  CAS  Google Scholar 

  • Bai, J. H., Baldwin, E. A., Goodner, K. L., Mattheis, J. P., & Brecht, J. K. (2005). Response of four apple cultivars to 1-methylcyclopropene treatment and controlled atmosphere storage. HortScience, 40, 1534–1538.

    CAS  Google Scholar 

  • Bowen, J. H., & Watkins, C. B. (1997). Fruit maturity, carbohydrate and mineral content relationships with watercore in ‘Fuji’ apples. Postharvest Biology and Technology, 11, 31–38.

    Article  CAS  Google Scholar 

  • Brackmann, A., Streif, J., & Bangerth, F. (1993). 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, 243–247.

    CAS  Google Scholar 

  • Brady, C. J. (1987). Fruit ripening. Annual Reviews of Plant Physiology and Plant Molecular Biology, 38, 155–178.

    Article  CAS  Google Scholar 

  • Burda, S., Oleszek, W., & Lee, C. Y. (1990). Phenolic compounds and their changes in apples during maturation and cold storage. Journal of Agricultural and Food Chemistry, 38, 945–948.

    Article  CAS  Google Scholar 

  • Cantu, D., Greve, L. C., Lurie, S., & Labavitch, J. M. (2006). Detection of uronic oxidase activity in ripening peaches. Phytochemistry, 67, 13–18.

    Article  PubMed  CAS  Google Scholar 

  • Coseteng, M. Y., & Lee, C. Y. (1987). Changes in apple polyphenoloxidase and polyphenol concentrations in relation to degree of browning. Journal of Food Science, 52, 985–989.

    Article  CAS  Google Scholar 

  • de Castro, E., Barrett, D. M., Jobling, J., & Mitcham, E. J. (2008). Biochemical factors associated with a CO2-induced flesh browning disorder of Pink Lady apples. Postharvest Biology and Technology, 48, 182–191.

    Article  Google Scholar 

  • de Castro, E., Biasi, B., Mitcham, E., Tustin, S., Tanner, D., & Jobling, J. (2007). Carbon dioxide-induced flesh browning in Pink Lady apples. Journal of the American Society for Horticultural Science, 132, 713–719.

    Google Scholar 

  • DeEll, J. R., Ayres, J. T., & Murr, D. P. (2007). 1-Methylcyclopropene influences ‘Empire’ and ‘Delicious’ apple quality during long-term commercial storage. HortTechnology, 17, 46–51.

    CAS  Google Scholar 

  • Defilippi, B. G., Dandekar, A. M., & Kader, A. A. (2004). Impact of suppression of ethylene action or biosynthesis on flavor metabolites in apple (Malus domestica Borkh) fruits. Journal of Agricultural and Food Chemistry, 52, 5694–5701.

    Article  PubMed  CAS  Google Scholar 

  • Defilippi, B. G., Dandekar, A. M., & Kader, A. A. (2005a). Relationship of ethylene biosynthesis to volatile production, related enzymes, and precursor availability in apple peel and flesh tissues. Journal of Agricultural and Food Chemistry, 53, 3133–3141.

    Article  PubMed  CAS  Google Scholar 

  • Defilippi, B. G., Kader, A. A., & Dandekar, A. M. (2005b). Apple aroma: Alcohol acyltransferase, a rate limiting step for ester biosynthesis, is regulated by ethylene. Plant Science, 168, 1199–1210.

    Article  CAS  Google Scholar 

  • Dong, S., Scagel, C. F., Cheng, L., Fuchigami, L. H., & Rygiewicz, P. T. (2001). Soil temperature and plant growth stage influence nitrogen uptake and amino acid concentration of apple during early spring growth. Tree Physiology, 21, 541–547.

    Article  PubMed  CAS  Google Scholar 

  • Drake, S. R., & Eisele, T. A. (1999). Carbohydrate and acid contents of Gala apples and Bartlett pears from regular and controlled atmosphere storage. Journal of Agricultural and Food Chemistry, 47, 3181–3184.

    Article  PubMed  CAS  Google Scholar 

  • Echeverría, G., Fuentes, T., Graell, J., Lara, I., & López, M. L. (2004). Aroma volatile compounds of ‘Fuji’ apples in relation to harvest date and cold storage technology: A comparison of two seasons. Postharvest Biology and Technology, 32, 29–44.

    Article  Google Scholar 

  • Elgar, H. J., Burmeister, D. M., & Watkins, C. B. (1998). Storage and handling effects on a CO2-related internal browning disorder of `Braeburn’ apples. HortScience, 33, 719–722.

    Google Scholar 

  • Fan, X., Blankenship, S. M., & Mattheis, J. P. (1999a). 1-Methylcyclopropene inhibits apple ripening. Journal of the American Society for Horticultural Science, 124, 690–695.

    CAS  Google Scholar 

  • Fan, X., & Mattheis, J. P. (1999). Impact of 1-methylcyclopropene and methyl jasmonate on apple volatile production. Journal of Agricultural and Food Chemistry, 47, 2847–2853.

    Article  PubMed  CAS  Google Scholar 

  • Fan, X., Mattheis, J. P., & Blankenship, S. (1999b). Development of apple superficial scald, soft scald, core flush, and greasiness is reduced by MCP. Journal of Agricultural and Food Chemistry, 47, 3063–3068.

    Article  PubMed  CAS  Google Scholar 

  • Fawbush, F., Nock, J. F., & Watkins, C. B. (2008). External carbon dioxide injury and 1-methylcyclopropene (1-MCP) in the ‘Empire’ apple. Postharvest Biology and Technology, 48, 92–98.

    Article  CAS  Google Scholar 

  • Fellman, J. K., Mattinson, D. S., Bostick, B. C., Mattheis, J. P., & Patterson, M. E. (1993). Ester biosynthesis in ‘Rome’ apples subjected to low-oxygen atmospheres. Postharvest Biology and Technology, 3, 201–214.

    Article  CAS  Google Scholar 

  • Fellman, J. K., Miller, T. W., Mattinson, D. S., & Mattheis, J. P. (2000). Factors that influence biosynthesis of volatile flavor compounds in apple fruits. HortScience, 35, 1026–1033.

    CAS  Google Scholar 

  • Ferenczi, A., Song, J., Tian, M., Vlachonasios, K., Dilley, D., & Beaudry, R. (2006). Volatile ester suppression and recovery following 1-methylcyclopropene application to apple fruit. Journal of the American Society for Horticultural Science, 131, 691–701.

    CAS  Google Scholar 

  • Fernández-Trujillo, J. P., Nock, J. F., & Watkins, C. B. (2001). Superficial scald, carbon dioxide injury, and changes of fermentation products and organic acids in ‘Cortland’ and ‘Law Rome’ apples after high carbon dioxide stress treatment. Journal of the American Society for Horticultural Science, 126, 235–241.

    Google Scholar 

  • Fidler, J. C., & North, C. J. (1970). Sorbitol in stored apples. Journal of Horticultural Science, 45, 197–204.

    CAS  Google Scholar 

  • Franck, C., Lammerteyn, J., & Nicolaï, B. (2005). Metabolic profiling using GC-MS to study biochemical changes during long-term storage of pears. Acta Horticulturae, 682, 1991–1998.

    CAS  Google Scholar 

  • Frenkel, C., Peters, J. S., Tieman, D. M., Tiznado, M. E., & Handa, A. K. (1998). Pectin methylesterase regulates methanol and ethanol accumulation in ripening tomato (Lycopersicon esculentum) fruit. Journal of Biological Chemistry, 273, 4293–4295.

    Article  PubMed  CAS  Google Scholar 

  • Fukuda, H. (1984). Relationship of watercore and calcium to the incidence of internal storage disorders of cultivar Fuji apple fruit. Journal of the Japanese Society for Horticultural Science, 53, 298–302.

    Article  Google Scholar 

  • Hansen, K., & Poll, L. (1993). Conversion of l-isoleucine into 2-methylbut-2-enyl esters in apples. Lebensmittel Wissenschaft und Technologie, 26, 178–180.

    CAS  Google Scholar 

  • Hulme, A. C. (1956). Carbon dioxide injury and the presence of succinic acid in apples. Nature, 178, 218–219.

    Article  CAS  Google Scholar 

  • Hulme, A. C., & Wooltorton, L. S. C. (1957). The organic acid metabolism of apple fruits: Changes in individual acids during growth on the tree. Journal of the Science of Food and Agriculture, 8, 117–122.

    Article  CAS  Google Scholar 

  • Ingle, M., D’Souza, M. C., & Townsend, E. C. (2000). Fruit characteristics of ‘York’ apples during development and after storage. HortScience, 35, 95–98.

    Google Scholar 

  • Jung, S.-K., & Watkins, C. B. (2011). Involvement of ethylene in browning development of controlled atmosphere-stored ‘Empire’ apple fruit. Postharvest Biology and Technology, 59, 219–226.

    Article  CAS  Google Scholar 

  • Kami, D., Muro, T., & Sugiyama, K. (2011). Changes in starch and soluble sugar concentrations in winter squash mesocarp during storage at different temperatures. Scientia Horticulturae, 127, 444–446.

    Article  CAS  Google Scholar 

  • Kondo, S., Setha, S., Rudell, D. R., Buchanan, D. A., & Mattheis, J. P. (2005). Aroma volatile biosynthesis in apples affected by 1-MCP and methyl jasmonate. Postharvest Biology and Technology, 36, 61–68.

    Article  CAS  Google Scholar 

  • Larrigaudière, C., Vilaplana, R., Soria, Y., & Recasens, I. (2008). Comparative study of the effects of 1-MCP treatment on apple quality by instrumental and multivariate analysis. Journal of the Science of Food and Agriculture, 88, 1614–1621.

    Article  Google Scholar 

  • Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., & Fernie, A. R. (2006). Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols, 1, 387–396.

    Article  PubMed  CAS  Google Scholar 

  • Magné, C., Bonenfant-Magné, M., & Audran, J.-C. (1997). Nitrogenous indicators of postharvest ripening and senescence in apple fruit (Malus domestica Borkh. cv. Granny Smith). International Journal of Plant Sciences, 158, 811–817.

    Article  Google Scholar 

  • Magné, C., & Larher, F. (1992). High sugar content of extracts interferes with colorimetric determination of amino acids and free proline. Analytical Biochemistry, 200, 115–118.

    Article  PubMed  Google Scholar 

  • Marlow, G. C., & Loescher, W. H. (1984). Watercore. Horticultural Reviews, 6, 189–251.

    CAS  Google Scholar 

  • Matich, A., & Rowan, D. (2007). Pathway analysis of branched-chain ester biosynthesis in apple using deuterium labeling and enantioselective gas chromatography-mass spectrometry. Journal of Agricultural and Food Chemistry, 55, 2727–2735.

    Article  PubMed  CAS  Google Scholar 

  • Mattheis, J. P. (2008). How 1-methylcyclopropene has altered the Washington state apple industry. HortScience, 43, 99–101.

    CAS  Google Scholar 

  • Mattheis, J. P., Buchanan, D. A., & Fellman, J. K. (1998). Volatile compounds emitted by ‘Gala’ apples following dynamic atmosphere storage. Journal of the American Society of Horticultural Science, 123, 426–432.

    CAS  Google Scholar 

  • Mattheis, J. P., Fan, X., & Argenta, L. C. (2005). Interactive responses of gala apple fruit volatile production to controlled atmosphere storage and chemical inhibition of ethylene action. Journal of Agricultrual and Food Chemistry, 53, 4510–4516.

    Article  CAS  Google Scholar 

  • Mayr, U., Treutter, D., Santos-Buelga, C., Bauer, H., & Feucht, W. (1995). Developmental changes in the phenol concentrations of ‘Golden Delicious’ apple fruits and leaves. Phytochemistry, 38, 1151–1155.

    Article  PubMed  CAS  Google Scholar 

  • McGuire, R. G. (1992). Reporting of objective color measurements. HortScience, 27, 1254–1255.

    Google Scholar 

  • Mir, N. A., & Beaudry, R. (1998). Effect of superficial scald suppression by diphenylamine application on volatile evolution by stored Cortland apple fruit. Journal of Agricultural and Food Chemistry, 47, 7–11.

    Article  Google Scholar 

  • Moya-Leon, M. A., Vergara, M., Bravo, C., Pereira, M., & Moggia, C. (2007). Development of aroma compounds and sensory quality of ‘Royal Gala’ apples during storage. Journal of Horticultural Science and Biotechnology, 82, 403–413.

    CAS  Google Scholar 

  • Pedreschi, R., Franck, C., Lammertyn, J., Erban, A., Kopka, J., Hertog, M., et al. (2009). Metabolic profiling of ‘Conference’ pears under low oxygen stress. Postharvest Biology and Technology, 51, 123–130.

    Article  CAS  Google Scholar 

  • Pérez-Enciso, M., & Tenenhaus, M. (2003). Prediction of clinical outcome with microarray data: A partial least squares discriminant analysis (PLS-DA) approach. Human Genetics, 112, 581–592.

    PubMed  Google Scholar 

  • Prasanna, V., Prabha, T. N., & Tharanathan, R. N. (2007). Fruit ripening phenomena—An overview. Critical Reviews in Food Science and Nutrition, 47, 1–19.

    Article  PubMed  CAS  Google Scholar 

  • Roessner, U., Luedemann, A., Brust, D., Fiehn, O., Linke, T., Willmitzer, L., et al. (2001). Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell, 13, 11–29.

    PubMed  CAS  Google Scholar 

  • Roessner, U., Wagner, C., Kopka, J., Trethewey, R. N., & Willmitzer, L. (2000). Simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant Journal, 23, 131–142.

    Article  PubMed  CAS  Google Scholar 

  • Rouchaud, J., Moons, C., & Meyer, J. A. (1985). Cultivar differences in the influence of harvest date and cold storage on the free sugars and acids contents, and on the eating quality of apples. Journal of Horticultural Science, 60, 291–296.

    CAS  Google Scholar 

  • Rowan, D. D., Lane, H. P., Allen, J. M., Fielder, S., & Hunt, M. B. (1996). Biosynthesis of 2-methylbutyl, 2-methyl-2-butenyl, and 2-methylbutanoate esters in Red Delicious and Granny Smith apples using deuterium-labeled substrates. Journal of Agricultural and Food Chemistry, 44, 3276–3285.

    Article  CAS  Google Scholar 

  • Rudell, D. R., Mattheis, J. P., & Curry, E. A. (2008). Prestorage ultraviolet–white light irradiation alters apple peel metabolome. Journal of Agricultural and Food Chemistry, 56, 1138–1147.

    Article  PubMed  CAS  Google Scholar 

  • Rudell, D. R., Mattheis, J. P., & Hertog, M. L. (2009). Metabolomic change precedes apple superficial scald symptoms. Journal of Agricultural and Food Chemistry, 57, 8459–8466.

    Article  PubMed  CAS  Google Scholar 

  • Rupasinghe, H. P. V., Murr, D. P., Paliyath, G., & Skog, L. (2000). Inhibitory effect of 1-MCP on ripening and superficial scald development in ‘McIntosh’ and ‘Delicious’ apples. Journal of Horticultural Science and Biotechnology, 75, 271–276.

    CAS  Google Scholar 

  • Sisler, E. C., & Serek, M. (1997). Inhibitors of ethylene responses in plants at the receptor level: Recent developments. Physiologia Plantarum, 100, 577–582.

    Article  CAS  Google Scholar 

  • Smagula, J. M., & Bramlage, W. J. (1977). Acetaldehyde accumulation: Is it a cause of physiological deterioration of fruits? HortScience, 12, 200–204.

    CAS  Google Scholar 

  • Smagula, J. M., Bramlage, W. J., Southwick, R. A., & Marsh, H. V. J. (1968). Effects of watercore on respiration and mitochondrial activity in ‘Richard Delicious’ apples. Proceedings of the American Society for Horticultural Science, 93, 753–761.

    CAS  Google Scholar 

  • Streif, J., & Bangerth, F. (1988). Production of volatile aroma substances by ‘Golden Delicious’ apple fruits after storage for various times in different CO2 and O2 concentrations. Journal of Horticultural Science, 63, 193–199.

    CAS  Google Scholar 

  • Suni, M., Nyman, M., Eriksson, N.-A., Björk, L., & Björck, I. (2000). Carbohydrate composition and content of organic acids in fresh and stored apples. Journal of the Science of Food and Agriculture, 80, 1538–1544.

    Article  CAS  Google Scholar 

  • Tsantili, E., Gapper, N. E., Arquiza, J., Whitaker, B. D., & Watkins, C. B. (2007). Ethylene and alpha-farnesene metabolism in green and red skin of three apple cultivars in response to 1-methylcyclopropene (1-MCP) treatment. Journal of Agricultural and Food Chemistry, 55, 5267–5276.

    Article  PubMed  CAS  Google Scholar 

  • Volz, R. K., Biasi, W. V., & Mitcham, E. J. (1998). Fermentative volatile production in relation to carbon dioxide-induced flesh browning in ‘Fuji’ apple. HortScience, 33, 1231–1234.

    CAS  Google Scholar 

  • Watkins, C. B. (2003). Principles and practices of postharvest handling and stress. In D. C. Ferree & I. J. Warrington (Eds.), Apple: Botany, production and uses (pp. 585–614). Wallingford: CAB International.

    Chapter  Google Scholar 

  • Watkins, C. B. (2006). The use of 1-methylcyclopropene (1-MCP) on fruits and vegetables. Biotechnology Advances, 24, 389–409.

    Article  PubMed  CAS  Google Scholar 

  • Watkins, C. B. (2007). The effect of 1-MCP on the development of physiological storage disorders in horticultural crops. Stewart Postharvest Review, 2, 1–6.

    Article  Google Scholar 

  • Watkins, C. B. (2008). Overview of 1-methylcyclopropene trials and uses for edible horticultural crops. HortScience, 43, 86–94.

    CAS  Google Scholar 

  • Watkins, C. B., & Liu, F. W. (2010). Temperature and carbon dioxide interactions on quality of controlled atmosphere-stored ‘Empire’ apples. HortScience, 45, 1708–1712.

    Google Scholar 

  • Watkins, C. B., Nock, J. F., & Whitaker, B. D. (2000). Responses of early, mid and late season apple cultivars to postharvest application of 1-methylcyclopropene (1-MCP) under air and controlled atmosphere storage conditions. Postharvest Biology and Technology, 19, 17–32.

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Jackie Nock at the Department of Horticulture, Cornell University, and David Buchanan and Rachel Leisso at USDA-ARS, Tree Fruit Research Laboratory, for their assistance. This research was partly supported by Federal Formula Funds NE1036, the New York Apple Research and Development Program, and AgroFresh, Inc. Jinwook Lee was supported by a Department of Horticulture assistantship.

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  1. Jinwook Lee

    Present address: USDA-ARS, Tree Fruit Research Laboratory, 1104 N. Western Avenue, Wenatchee, WA, 98801, USA

Authors and Affiliations

  1. Department of Horticulture, Cornell University, Ithaca, NY, 14853, USA

    Jinwook Lee & Christopher B. Watkins

  2. USDA-ARS, Tree Fruit Research Laboratory, 1104 N. Western Avenue, Wenatchee, WA, 98801, USA

    David R. Rudell

  3. Department of Plant Biology and Horticulture, Cornell University, Ithaca, NY, 14853, USA

    Peter J. Davies

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Lee, J., Rudell, D.R., Davies, P.J. et al. Metabolic changes in 1-methylcyclopropene (1-MCP)-treated ‘Empire’ apple fruit during storage. Metabolomics 8, 742–753 (2012). https://doi.org/10.1007/s11306-011-0373-5

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