Abstract
Cold storage can effectively delay the ripening of ‘Nanguo’ pears (Pyrus ussuriensis Maxim.). However, the aroma-related esters of ‘Nanguo’ pears decreased after cold storage. In this study, we aimed to investigate the effect of intermittent warming (IW) treatment on the formation of aroma-related esters and unsaturated fatty acid synthesis from cold stored pears. IW-treated pears were exposed to 20 ± 1 °C for 1 day every 20 days during storage at 0 ± 0.5 °C, every 21 days was a cycle and a total of 90 days. The pears in control group were stored at 0 ± 0.5 °C for 90 days. After this 90-day storage, both groups of pears (control and IW-treated) were transferred to a shelf life of 12 days at room temperature. The results showed that, compared with the pears in control group, the productions of aroma-related esters and the expression levels of PuLOX1, PuADH3, and PuAAT1 in IW-treated pears were significantly higher during the shelf life (P < 0.05). At the same time, IW-treated pears maintained significantly higher contents of linoleic acid and linolenic acid (P < 0.05), which were precursors of aroma compounds. We also found that the expression of PuFAD2 and PuFAD3 had significant positive correlation with the contents of unsaturated fatty acids (P < 0.05). The significantly higher expression levels of PuFAD2 and PuFAD3 in IW-treated pears may have played an important role in the improvement of ester contents (P < 0.05). It could be inferred that IW treatment had an impact on the aroma-related esters of cold-stored ‘Nanguo’ pears through regulation of unsaturated fatty acid synthesis.
Similar content being viewed by others
References
Aghdam, M. S., & Bodbodak, S. (2014). Postharvest heat treatment for mitigation of chilling injury in fruits and vegetables. Food and Bioprocess Technology, 7(1), 37–53.
Alwan, T. F., & Watkins, C. B. (1999). Intermittent warming effects on superficial scald development of ‘Cortland’, ‘delicious’ and ‘law Rome’ apple fruit. Postharvest Biology and Technology, 16(3), 203–212.
Artés, F., Cano, A., & Fernández-Trujillo, J. P. (1996). Pectolytic enzyme activity during intermittent warming storage of peaches. Journal of Food Science, 61(2), 311–314.
Artés, F., Sánchez, E., & Tijskens, L. M. M. (1998). Quality and shelf life of tomatoes improved by intermittent warming. LWT- Food Science and Technology, 31(5), 427–431.
Axelrod, B., Cheesbrough, T. M., & Leakso, S. (1981). Lipoxygenase from soybeans. Methods in Enzymology, 7, 441–451.
Biswas, P., East, A. R., Hewett, E. W., & Heyes, J. A. (2010). Intermittent warming interactions on the ripening of green mature tomatoes. Acta Horticulturae, 800, 153–160.
Biswas, P., East, A. R., Brecht, J. K., Hewett, E. W., & Heyes, J. A. (2012). Intermittent warming during low temperature storage reduces tomato chilling injury. Postharvest Biology and Technology, 74, 71–78.
Biswas, P., East, A. R., Hewett, E. W., & Heyes, J. A. (2016). Intermittent warming in alleviating chilling injury—a potential technique with commercial constraint. Food and Bioprocess Technology, 9(1), 1–15.
Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37(8), 911–917.
Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254.
Brian, F., Alberto, A. A., Fotios, G. P., Simona, M. C., Guglielmo, C., Frans, J. M. H., & Ernst, J. W. (2015). Chilling-induced changes in aroma volatile profiles in tomato. Food and Bioprocess Technology, 8, 1442–1454.
Buttery, R. G., Teranishi, R., & Ling, L. C. (1987). Fresh tomato aroma volatiles: a quantitative study. Journal of Agricultural and Food Chemistry, 35(4), 540–544.
Canoles, M. A., & Beaudry, R. M. (2006). Deficiency of linolenic acid in Lefad7 mutant tomato changes the volatile profile and sensory perception of disrupted leaf and fruit tissue. Journal of the American Society for Horticultural Science, 131(2), 284–289.
Cao, S., Zheng, Y., Wang, K., Jin, P., & Rui, H. (2009). Methyl jasmonate reduces chilling injury and enhances antioxidant enzyme activity in postharvest loquat fruit. Food Chemistry, 115(4), 1458–1463.
Cheng, S. C., Wei, B. D., Zhou, Q., Tan, D. H., & Ji, J. S. (2015). 1-Methylcyclopropene alleviates chilling injury by regulating energy metabolism and fatty acid content in ‘Nanguo’ pears. Postharvest Biology and Technology, 109, 130–136.
Goff, S. A., & Klee, H. J. (2006). Plant volatile compounds: sensory cues for health and nutritional value. Science, 311(5762), 815–819.
Hatanaka, A. (1993). The biogeneration of green odour by green leaves. Phytochemistry, 34(5), 1201–1218.
Hernández, M. L., Padilla, M. N., Sicardo, M. D., Mancha, M., & Martínez-Rivas, J. M. (2011). Effect of different environmental stresses on the expression of oleate desaturase genes and fatty acid composition in olive fruit. Phytochemistry, 72(2-3), 178–187.
Infante, R., Farcuh, M., & Meneses, C. (2008). Monitoring the sensorial quality and aroma through an electronic nose in peaches during cold storage. Journal of the Science of Food and Agriculture, 88(12), 2073–2078.
Jannatizadeh, A., Aghdam, M. S., Luo, Z., & Razavi, F. (2019). Impact of exogenous melatonin application on chilling injury in tomato fruits during cold storage. Food and Bioprocess Technology, 12(5), 741–750.
Ke, D. Y., Zhou, L. L., & Kader, A. A. (1994). Mode of oxygen and carbon dioxide action on strawberry ester biosynthesis. Journal of the American Society for Horticultural Science, 119(5), 971–975.
Li, T., Li, X., Tan, D., Jiang, Z., Wei, Y., Li, J., Du, G., & Wang, A. (2014). Distinct expression profiles of ripening related genes in the ‘Nanguo’ pear (Pyrus ussuriensis) fruit. Science Horticulturae, 171, 78–82.
Liu, L., Wei, Y. N., Shi, F., Liu, C., Liu, X. C., & Ji, S. J. (2015). Intermittent warming improves postharvest quality of bell peppers and reduces chilling injury. Postharvest Biology and Technology, 101, 18–25.
Luo, M. L., Zhou, X., Sun, H. J., Zhou, Q., Wei, B. D., Cheng, S. C., & Ji, S. J. (2020). Glycine betaine treatment alleviates loss of aroma-related esters in cold-stored ‘Nanguo’ pears by regulating the lipoxygenase pathway. Food Chemistry, 316, 126335.
Mirdehghan, S. H., Rahemi, M., Martínez-Romero, D., Guillén, F., Valverde, J. M., Zapata, P. J., Serrano, M., & Valero, D. (2007). Reduction of pomegranate chilling injury during storage after heat treatment: role of polyamines. Postharvest Biology and Technology, 44(1), 19–25.
Paillard, N. M. M., & Rouri, O. (1984). Hexanal and 2-hexenal production by mashed apple tissues. Lebensm-Wiss Technology, 17, 345–350.
Pérez, A. G., Sanz, C., Olías, R., Ríos, J. J., & Olías, J. M. (1996). Evolution of strawberry alcohol acyltransferase activity during fruit development and storage. Journal of Agricultural and Food Chemistry, 44(10), 3286–3290.
Purwanto, Y. A., Budiastra, I. W., & Darmawati, E. (2016). Effect of low temperature storage on the ripe-stage eating period of ‘Gedong Gincu’ mango fruit. ARPN Journal of Engineering and Applied Sciences, 11, 10365–10367.
Qin, G. H., Tao, S. T., Zhang, H. P., Huang, W. J., Wu, J. Y., Xu, Y. L., & Zhang, S. L. (2014). Evolution of the aroma volatiles of pear fruits supplemented with fatty acid metabolic precursors. Molecules, 19(12), 20183–20196.
Sapitnitskaya, M., Maul, P., McCollum, G. T., Guy, C. L., Weiss, B., Samach, A., & Porat, R. (2006). Postharvest heat and conditioning treatments activate different molecular responses and reduce chilling injuries in grapefruit. Journal of Experimental Botany, 57(12), 2943–2953.
Schwab, W., Davidovich-Rikanati, R., & Lewinsohn, E. (2008). Biosynthesis of plant derived flavor compounds. Plant Journal, 54(4), 712–732.
Shi, F., Zhou, X., Zhou, Q., Tan, Z., Yao, M. M., Wei, B. D., & Ji, S. J. (2018a). Membrane lipid metabolism changes and aroma ester loss in low-temperature stored Nanguo pears. Food Chemistry, 245, 446–453.
Shi, F., Zhou, X., Zhou, Q., Tan, Z., Yao, M. M., Wei, B. D., & Ji, S. J. (2018b). Transcriptome analyses provide new possible mechanisms of aroma ester weakening of ‘Nanguo’ pears after refrigeration. Science Horticulturae, 237, 247–256.
Sun, Y., Gu, X., Sun, K., Hu, H., Xu, M., Wang, Z., Tu, K., & Pan, L. (2017). Hyperspectral reflectance imaging combined with chemometrics and successive projections algorithm for chilling injury classification in peaches. LWT- Food Science and Technology, 75, 557–564.
Takeoka, G. R., Flath, R. A., Buttery, R. G., Winterhalter, P., Güntert, M., Ramming, D. W., & Teranishi, R. (1992). Free and bound flavor constituents of white-fleshed nectarines. American Chemical Society, 10, 116–138.
Wang, C. L., Chin, C. K., Ho, C. T., Hwang, C. F., Polashock, J. J., & Martin, C. E. (1996). Changes of fatty acids and fatty acid-derived flavor compounds by expressing the yeast Δ-9 desaturase gene in tomato. Journal of Agricultural and Food Chemistry, 44(10), 3399–3402.
Wang, C. L., Xing, J. S., Chin, C. K., Ho, C. T., & Martin, C. E. (2001). Modification of fatty acids changes the flavor volatiles in tomato leaves. Phytochemistry, 58(2), 227–232.
Wang, X. J., Beno-Moualemd, D., Kobiler, I., Leikin-Frenkel, A., Liehter, A., & Prusky, D. (2004). Expression of Δ12 fatty acid desaturase during the induced accumulation of the antifungal diene in avocado fruit. Molecular Plant Pathology, 5(6), 575–585.
Wang, J. W., Lv, M., Li, G. D., Jiang, Y. G., Fu, W. W., Zhang, L., & Ji, S. J. (2018). Effect of intermittent warming on alleviation of peel browning of ‘Nanguo’ pears by regulation energy and lipid metabolisms after cold storage. Postharvest Biology and Technology, 142, 99–106.
Watkins, C. B. (2002). Ethylene synthesis, mode of action, consequences and control. In M. Knee (Ed.), Fruit quality and its biological basis (pp. 180–224). Boca Raton, FL: CRC Press.
Wei, S. W., Qin, G. H., Zhang, H. P., Tao, S. T., Wu, J., Wang, S. M., & Zhang, S. L. (2017). Calcium treatments promote the aroma volatiles emission of pear (Pyrus ussuriensis ‘Nanguoli’) fruit during post-harvest ripening process. Science Horticulturae, 215, 102–111.
Wu, Q., Liu, T., Liu, H., & Zheng, G. C. (2009). Unsaturated fatty acid: metabolism, synthesis and gene regulation. African Journal of Biotechnology, 8(9), 1782–1785.
Xi, W.P., Zhang, B., Shen, J.Y., Sun, C.D, Xu, C.J., & Chen, K.S. (2012). Intermittent warming alleviated the loss of peach fruit aroma-related esters by regulation of AAT during cold storage. Postharvest Biology and Technology, 74, 42–48.
Yi, X. K., Liu, G. F., Rana, M. M., Zhu, L. W., Jiang, S. L., Huang, Y. F., Lu, W. M., & Wei, S. (2016). Volatile profiling of two pear genotypes with different potential for white pear aroma improvement. Science Horticulturae, 209, 221–228.
Zhang, C. F., & Tian, S. P. (2009). Crucial contribution of membrane lipids’ unsaturation to acquisition of chilling-tolerance in peach fruit stored at 0°C. Food Chemistry, 115(2), 405–411.
Zhang, B., Shen, J. Y., Wei, W. W., Xi, W. P., Xu, C. J., Ferguson, I., & Chen, K. S. (2010). Expression of genes associated with aroma formation derived from the fatty acid pathway during peach fruit ripening. Journal of Agricultural and Food Chemistry, 58(10), 6157–6165.
Zhang, B., Xi, W. P., Wei, W. W., Shen, J. Y., Ferguson, I., & Chen, K. S. (2011). Changes in aroma-related volatiles and gene expression during low temperature storage and subsequent shelf-life of peach fruit. Postharvest Biology and Technology, 60(1), 7–16.
Zhang, L., Wang, J. W., Li, G. D., Zhou, X., Fu, W. W., Jiang, Y. G., Liu, T., & Ji, S. J. (2018). Exogenous ATP alleviated aroma fading by regulating LOX pathway and fatty acids synthesis in ‘Nanguo’ pears after refrigeration. Science Horticulturae, 240, 522–529.
Zhou, X., Dong, L., Zhou, Q., Wang, J. W., Nan, C., Liu, Z. Y., & Ji, S. J. (2015a). Effects of intermittent warming on aroma-related esters of 1-methylcyclopropene-treated ‘Nanguo’ pears during ripening at room temperature. Science Horticulturae, 185, 82–89.
Zhou, X., Dong, L., Li, R., Zhou, Q., Wang, J. W., & Ji, S. J. (2015b). Low temperature conditioning prevents loss of aroma-related esters from ‘Nanguo’ pear during ripening at room temperature. Postharvest Biology and Technology, 100, 23–32.
Zou, J., Chen, J., Tang, N., Gao, Y., Hong, M., Wei, W., Cao, H., Jian, W., Li, N., Deng, W., & Li, Z. (2018). Transcriptome analysis of aroma volatile metabolism change in tomato (Solanum lycopersicum) fruit under different storage temperatures and 1-MCP treatment. Postharvest Biology and Technology, 135, 57–67.
Funding
The National Natural Science Foundation funded this project (No. 31971698).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Zhou, X., Tan, Z., Zhou, Q. et al. Effect of Intermittent Warming on Aroma-Related Esters of ‘Nanguo’ Pears Through Regulation of Unsaturated Fatty Acid Synthesis After Cold Storage. Food Bioprocess Technol 13, 1119–1130 (2020). https://doi.org/10.1007/s11947-020-02469-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11947-020-02469-y