Metabolomics

, Volume 8, Issue 4, pp 742–753 | Cite as

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

  • Jinwook Lee
  • David R. Rudell
  • Peter J. Davies
  • Christopher B. Watkins
Original Article

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.

Keywords

Metabolomics Partial least squares analysis (PLS) GC–MS Sorbitol GABA Amino acids Volatiles Phenolic compounds Flesh browning 

Supplementary material

11306_2011_373_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 19 kb)

References

  1. 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.CrossRefGoogle Scholar
  2. 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.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. 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.Google Scholar
  5. 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.PubMedCrossRefGoogle Scholar
  6. 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.Google Scholar
  7. 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.CrossRefGoogle Scholar
  8. 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.Google Scholar
  9. Brady, C. J. (1987). Fruit ripening. Annual Reviews of Plant Physiology and Plant Molecular Biology, 38, 155–178.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. Cantu, D., Greve, L. C., Lurie, S., & Labavitch, J. M. (2006). Detection of uronic oxidase activity in ripening peaches. Phytochemistry, 67, 13–18.PubMedCrossRefGoogle Scholar
  12. 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.CrossRefGoogle Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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
  15. 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.Google Scholar
  16. 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.PubMedCrossRefGoogle Scholar
  17. 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.PubMedCrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.PubMedCrossRefGoogle Scholar
  20. 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.PubMedCrossRefGoogle Scholar
  21. 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.CrossRefGoogle Scholar
  22. 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
  23. 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.Google Scholar
  24. 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.PubMedCrossRefGoogle Scholar
  25. 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.PubMedCrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.Google Scholar
  29. 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.Google Scholar
  30. 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
  31. Fidler, J. C., & North, C. J. (1970). Sorbitol in stored apples. Journal of Horticultural Science, 45, 197–204.Google Scholar
  32. 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.Google Scholar
  33. 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.PubMedCrossRefGoogle Scholar
  34. 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.CrossRefGoogle Scholar
  35. Hansen, K., & Poll, L. (1993). Conversion of l-isoleucine into 2-methylbut-2-enyl esters in apples. Lebensmittel Wissenschaft und Technologie, 26, 178–180.Google Scholar
  36. Hulme, A. C. (1956). Carbon dioxide injury and the presence of succinic acid in apples. Nature, 178, 218–219.CrossRefGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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
  39. 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.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. 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.CrossRefGoogle Scholar
  43. 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.PubMedCrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. 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.PubMedCrossRefGoogle Scholar
  46. Marlow, G. C., & Loescher, W. H. (1984). Watercore. Horticultural Reviews, 6, 189–251.Google Scholar
  47. 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.PubMedCrossRefGoogle Scholar
  48. Mattheis, J. P. (2008). How 1-methylcyclopropene has altered the Washington state apple industry. HortScience, 43, 99–101.Google Scholar
  49. 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.Google Scholar
  50. 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.CrossRefGoogle Scholar
  51. 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.PubMedCrossRefGoogle Scholar
  52. McGuire, R. G. (1992). Reporting of objective color measurements. HortScience, 27, 1254–1255.Google Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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.Google Scholar
  55. 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.CrossRefGoogle Scholar
  56. 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.PubMedGoogle Scholar
  57. Prasanna, V., Prabha, T. N., & Tharanathan, R. N. (2007). Fruit ripening phenomena—An overview. Critical Reviews in Food Science and Nutrition, 47, 1–19.PubMedCrossRefGoogle Scholar
  58. 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.PubMedGoogle Scholar
  59. 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.PubMedCrossRefGoogle Scholar
  60. 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.Google Scholar
  61. 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.CrossRefGoogle Scholar
  62. 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.PubMedCrossRefGoogle Scholar
  63. 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.PubMedCrossRefGoogle Scholar
  64. 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.Google Scholar
  65. Sisler, E. C., & Serek, M. (1997). Inhibitors of ethylene responses in plants at the receptor level: Recent developments. Physiologia Plantarum, 100, 577–582.CrossRefGoogle Scholar
  66. Smagula, J. M., & Bramlage, W. J. (1977). Acetaldehyde accumulation: Is it a cause of physiological deterioration of fruits? HortScience, 12, 200–204.Google Scholar
  67. 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.Google Scholar
  68. 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.Google Scholar
  69. 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.CrossRefGoogle Scholar
  70. 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.PubMedCrossRefGoogle Scholar
  71. 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.Google Scholar
  72. 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.CrossRefGoogle Scholar
  73. Watkins, C. B. (2006). The use of 1-methylcyclopropene (1-MCP) on fruits and vegetables. Biotechnology Advances, 24, 389–409.PubMedCrossRefGoogle Scholar
  74. 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.CrossRefGoogle Scholar
  75. Watkins, C. B. (2008). Overview of 1-methylcyclopropene trials and uses for edible horticultural crops. HortScience, 43, 86–94.Google Scholar
  76. 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
  77. 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.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Jinwook Lee
    • 1
    • 4
  • David R. Rudell
    • 2
  • Peter J. Davies
    • 3
  • Christopher B. Watkins
    • 1
  1. 1.Department of HorticultureCornell UniversityIthacaUSA
  2. 2.USDA-ARSTree Fruit Research LaboratoryWenatcheeUSA
  3. 3.Department of Plant Biology and HorticultureCornell UniversityIthacaUSA
  4. 4.USDA-ARSTree Fruit Research LaboratoryWenatcheeUSA

Personalised recommendations