Different Chilling-Induced Symptoms and the Underlying Oxidative Stress and Antioxidative Defense in the Exocarp and Mesocarp of Immature Sponge Gourd (Luffa cylindrica) Fruit
Article Sidebar
Published:
Jul 13, 2021
Keywords:
Ascorbic acid Antioxidant Chilling injury Cold stress Reactive oxygen species
Main Article Content
Abstract
Immature sponge gourd fruit is consumed as a vegetable with a limited shelf life. Although cold storage is a simple and powerful tool for maintaining postharvest fruit quality, storage at a low temperature may not be appropriate for vegetables as some chilling injury (CI) of the immature sponge gourd fruit may occur. Therefore, this research aimed to elucidate the relationship between CI, oxidative stress, and the antioxidative defense mechanisms in the exocarp and mesocarp of immature sponge gourd fruit. After storage at 5°C for 6 days, visual CI symptoms, including browning and surface pitting, were found in the peel (exocarp) but not in the mesocarp. There were, however, more dead cells (stained by Evans blue) in the mesocarp of the fruit stored at 5°C. There was a more considerable increase in the electrolyte leakage rate in both fruit tissues held at 5°C than 25°C. The CI was correlated with malondialdehyde (MDA) levels in the tissues. The MDA of fruit exocarp at 5°C was 1.6 fold higher than that at 25°C on day 6, while the lipoxygenase (LOX) activity in mesocarp was 50% higher in fruit stored at a lower temperature. The action of ascorbate peroxidase (APX) was high in the exocarp of the fruit stored at 5°C, but there appeared to be a continuous depletion of the co-substrate or ascorbic acid. In conclusion, the CI in the exocarp was mainly associated with a high level of reactive oxygen species (ROS). In contrast, the CI in the mesocarp appeared to be primarily associated with increased lipid peroxidation by the elevated LOX activity under cold stress compared to storage at 25°C.
Article Details
How to Cite
Chuenchom, P., Noichinda, S., Bodhipadma, K., Wongs-Aree, C., & Leung, D. W. M. (2021). Different Chilling-Induced Symptoms and the Underlying Oxidative Stress and Antioxidative Defense in the Exocarp and Mesocarp of Immature Sponge Gourd (Luffa cylindrica) Fruit. Applied Science and Engineering Progress, 14(3), 348–359. https://doi.org/10.14416/j.asep.2021.04.007
Issue
Section
Research Articles
References
[1] L. Jia, X. Qin, D. Lyu, S. Qin, and P. Zhang, “ROS production and scavenging in three cherry rootstocks under short-term waterlogging conditions,” Scientia Horticulturae, vol. 257, 2019, Art. no. 108647.
[2] W. Pongprayoon, T. Siringam, A, Panya, and S, Roytrakul, “Application of chitosan in plant defense responses to biotic and abiotic stresses,” Applied Science and Engineering Progress, 2020, doi: 10.14416/j.asep.2020.12.007.
[3] C. Wongs-Aree, P. Siripirom, A. Satitpongchai, K. Bodhipadma, and S. Noichinda, “Increasing lignification in translucent disorder aril of mangosteen related to the ROS defensive function,” Journal of Food Quality, 2021, Art. no. 6674208, doi: 10.1155/2021/6674208.
[4] C. Kaya, M. Ashraf, M. N. Alyemeni, F. J. Corpas, and P. Ahmad, “Salicylic acid-induced nitric oxide enhances arsenic toxicity tolerance in maize plants by upregulating the ascorbateglutathione cycle and glyoxalase system,” Journal of Hazardous Materials, vol. 399, Art. no. 123020, 2020.
[5] R. J. Zong, M. I. Cantwell, and L. L. Morris, “Postharvest handling of Asian specialty vegetables under study,” California Agriculture, vol. 47, pp. 27–29, 1993.
[6] A. Tewari, R. Singh, N. K. Singh, and U. N. Rai, “Amelioration of municipal sludge by Pistia stratiotes L.: Role of antioxidant enzymes in detoxification of metals,” Bioresource Technology, vol. 99, pp. 8715–8721, 2008, doi: 10.1016/j. biortech.2008.04.018.
[7] S. Phornvillay, N. Prongprasert, C. Wongs-Aree, A. Uthairatanakij, and V. Srilaong, “Physiobiochemical responses of okra (Abelmoschus esculentus) to oxidative stress under low temperature storage,” Horticulture Journal, vol. 89, pp. 69–77, 2020.
[8] H. Cen, R. Lu, Q. Zhu, and F. Mendoza, “Nondestructive detection of chilling injury in cucumber fruit using hyperspectral imaging with feature selection and supervised classification,” Postharvest Biology Technology, vol. 111, pp. 352–361, 2016, doi: 10.1016/j.postharvbio.2015.09.027.
[9] Y. Lu and R. Lu, “Enhancing chlorophyll fluorescence imaging under structured illumination with automatic vignetting correction for detection of chilling injury in cucumbers,” Computers and Electronics in Agriculture, vol. 168, p. 105145, 2020, doi: 10.1016/j.compag.2019.105145.
[10] K. Luengwilai and D. M. Beckles, “Effect of low temperature storage on fruit physiology and carbohydrate accumulation in tomato ripening– inhibited mutants,” Journal of Stored Products and Postharvest Research, vol. 4, pp. 35–43, 2013, doi: 10.5897/JSPPR10.012.
[11] L. Mao, G. Wang, C. Zhu, and H. Pang, “Involvement of phospholipase D and lipoxygenase in response to chilling stress in postharvest cucumber fruits,” Plant Science, vol. 172, pp. 400–405, 2007, doi: 10.1016/j.plantsci.2006.10.002.
[12] C. Han, J. Zuo, Q. Wang, H. Dong, and L. Gao, “Salicylic acid alleviates postharvest chilling injury of sponge gourd (Luffa cylindrica),” Journal of Integrative Agriculture, vol. 16, pp. 735–741, 2017, doi: 10.1016/S2095-3119(16)61390-4.
[13] C. J. Baker and M. N. Mock, “An improved method for monitoring cell death in cell suspension and leaf disc assays using evans blue,” Plant Cell, Tissue and Organ Culture, vol. 39, pp. 7–12, 1994, doi: 10.1007/BF00037585.
[14] S. Lutts, J. M. Kinect, and J. Bouharmont, “NaClinduced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance,” Annals of Botany, vol. 78, pp. 389–398, 1996, doi: 10.1006/anbo.1996. 0134.
[15] K. S. Krishan Chaitanya and S. C. Naithani, “Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn.f.,” New Phytologist, vol. 126, pp. 623–627, 1994, doi: 10.1111/ j.14698137.1994.tb02957.x.
[16] M. Zouari, C. B. Ahmed, W. Zorrig, N. Elloumi, M. Rabhi, D. Delmail, B. B. Rouina, P. Labrousse, and F. B. Abdallah, “Exogenous proline mediates alleviation of cadmium stress by promoting photosynthetic activity, water status and antioxidative enzymes activities of young date palm (Phoenix dactylifera L.),” Ecotoxicology and Environmental Safety, vol. 128, pp. 100–108, 2016, doi: 10. 1016/j.ecoenv.2016. 02.015.
[17] S. Dipierro and S. De Leonardis, “The ascorbate system and lipid peroxidation in stored potato (Solanum tuberosum L.) tubers,” Journal of Experimental Botany, vol. 48, pp. 779–783, 1997, doi: 10.1093/jxb/48.3.779.
[18] R. S. Dhindsa, P. Plumb-Dhindsa, and T. A. Thorpe, “Leaf senescence: Correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase,” Journal of Experimental Botany, vol. 32, pp. 93–101, 1981, doi: 10.1093/jxb/32.1.93.
[19] A. Jiménez, J. A. Hernández, L. A. del Rio, and F. Sevilla, “Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves,” Plant Physiology, vol. 114, pp. 275–284, 1997, doi: 10. 1104/pp.114.1.275.
[20] D. Martins and A. M. English, “Catalase activity is stimulated by H2O2 in rich culture medium and is required for H2O2 resistance and adaptation in yeast,” Redox Biology, vol. 2, 308–313, 2014, doi: 10.1016/j.redox. 2013.12.019.
[21] H. Song, X. Gao, B. Feng, H. Dai, P. Zhang, J. Gao, P. Wang, and Y. Chai, “Leaf senescence and physiological characters in different adzuki bean (Vigna angularis) cultivars (lines),” African Journal of Agricultural Research, vol. 8, pp. 4025–4032, 2013, doi: 10. 5897/AJAR11.1827.
[22] Y. Imahori, M. Takemura, and J. Bai, “Chilling– induced oxidative stress and antioxidant responses in mume (Prunus mume) fruit during low temperature storage,” Postharvest Biology Technology, vol. 49, pp. 54–60, 2008, doi: 10.1016/ j.postharvbio.2007.10.017.
[23] B. P. Klein and A. K. Perry, “Ascorbic acid and vitamin A activity in selected vegetables from different geographical areas of the United States,” Journal of Food Science, vol. 47, pp. 941–945, 1982, doi: 10.1111/j.1365-2621.1982.tb12750.x.
[24] R. J. Bruce and C. A. West, “Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean,” Plant Physiology, vol. 91, pp. 889–897, 1989, doi: 10.1104/pp.91.3.88.
[25] M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, pp. 248–254, 1976, doi: 10.1016/ 0003-2697(76)90527-3.
[26] C. N. Huang, M. J. Cornejo, D. S. Bush, and R. L. Jones, “Estimating viability of plant protoplasts using double and single staining,” Protoplasma, vol. 135, pp. 80–87, 1986.
[27] P. Vijayaraghavareddy, V. Adhinarayanreddy, R. S. Vemanna, S. Sreeman, and U. Makarla, “Quantification of membrane damage/cell death using Evan’s blue staining technique,” Bio- Protocol, vol. 7, pp. 1–8, 2017, doi: 10.21769/ BioProtoc.2519.
[28] S. S. Gill and N. Tuteja, “Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants,” Plant Physiology Biochemistry, vol. 48, pp. 909–930, 2010.
[29] J. Wong-ekkabut, Z. Xu, W. Triampo, I-M. Tang, D. P. Tieleman, and L. Monticelli, “Effect of lipid peroxidation on the properties of lipid bilayers: A molecular dynamics study,” Biophysical Journal, vol. 93, pp. 4225-4236, 2007, doi: 10.1529/ biophysj.107.112565.
[30] M. S. Aghdam and S. Bodbodak, “Physiological and biochemical mechanisms regulating chilling tolerance in fruits and vegetables under postharvest salicylates and jasmonates treatments,” Scientia Horticulturae, vol. 156, pp. 73–85, 2013, doi: 10. 1016/j.scienta.2013.03.028.
[31] R. L. Heath and L. Packer, “Photo peroxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation,” Archives of Biochemistry and Biophysics, vol. 125, pp. 189–198, 1968, doi: 10. 1016/0003-9861(68)90654-1.
[32] L. Mao, H. Pang, G. Wang, and C. Zhu “Phospholipase D and lipoxygenase activity of cucumber fruit in response to chilling stress,” Postharvest Biology Technology, vol. 44, pp. 42–47, 2007, doi: 10.1016/j.postharvbio.2006. 11.009.
[33] K. Fahmy, K. Nakano, and F. Violalita, “Investigation on quantitative index of chilling injury in cucumber fruit based on the electrolyte leakage and malondialdehyde content,” International Journal on Advanced Science, Engineering and Information Technology, vol. 5, pp. 222–225, 2015, doi: 10.18517/ ijaseit.5.3.532.
[34] P. Sharma, A. B. Jha, R. S. Dubey, and M. Pessarakli, “Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions,” Journal of Botany, vol. 2012, pp. 217037, 2012, doi: 10.1155/2012/ 217037.
[35] S. Noichinda, K. Bodhipadma, C. Mahamontri, T. Narongruk, and S. Ketsa, “Light during storage prevents loss of ascorbic acid, and increases glucose and fructose levels in Chinese kale (Brassica oleracea var. alboglabra),” Postharvest Biology Technology, vol. 44, pp. 312–315, 2007, doi: 10. 1016/j.postharvbio.2006.12.006.
[36] Y. Yabuta, T. Maruta, A. Nakamura, T. Mieda, K. Yoshimura, T. Ishikawa, and S. Shigeoka, “Conversion of L-galactono-1,4-lactone to Lascorbate is regulated by the photosynthetic electron transport chain in Arabidopsis,” Bioscience, Biotechnology, and Biochemistry, vol. 72, pp. 2598–2607, 2008, doi: 10.1271/bbb.80284
[37] R. Bhardwaj, N. Handa, R. Sharma, H. Kaur, S. Kohli, V. Kumar, and P. Kaur, “Lignins and abiotic stress: An overview,” in Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment, P. Ahmad, and M. R. Wani, Eds. New York: Springer, 2014, pp. 267–296.
[2] W. Pongprayoon, T. Siringam, A, Panya, and S, Roytrakul, “Application of chitosan in plant defense responses to biotic and abiotic stresses,” Applied Science and Engineering Progress, 2020, doi: 10.14416/j.asep.2020.12.007.
[3] C. Wongs-Aree, P. Siripirom, A. Satitpongchai, K. Bodhipadma, and S. Noichinda, “Increasing lignification in translucent disorder aril of mangosteen related to the ROS defensive function,” Journal of Food Quality, 2021, Art. no. 6674208, doi: 10.1155/2021/6674208.
[4] C. Kaya, M. Ashraf, M. N. Alyemeni, F. J. Corpas, and P. Ahmad, “Salicylic acid-induced nitric oxide enhances arsenic toxicity tolerance in maize plants by upregulating the ascorbateglutathione cycle and glyoxalase system,” Journal of Hazardous Materials, vol. 399, Art. no. 123020, 2020.
[5] R. J. Zong, M. I. Cantwell, and L. L. Morris, “Postharvest handling of Asian specialty vegetables under study,” California Agriculture, vol. 47, pp. 27–29, 1993.
[6] A. Tewari, R. Singh, N. K. Singh, and U. N. Rai, “Amelioration of municipal sludge by Pistia stratiotes L.: Role of antioxidant enzymes in detoxification of metals,” Bioresource Technology, vol. 99, pp. 8715–8721, 2008, doi: 10.1016/j. biortech.2008.04.018.
[7] S. Phornvillay, N. Prongprasert, C. Wongs-Aree, A. Uthairatanakij, and V. Srilaong, “Physiobiochemical responses of okra (Abelmoschus esculentus) to oxidative stress under low temperature storage,” Horticulture Journal, vol. 89, pp. 69–77, 2020.
[8] H. Cen, R. Lu, Q. Zhu, and F. Mendoza, “Nondestructive detection of chilling injury in cucumber fruit using hyperspectral imaging with feature selection and supervised classification,” Postharvest Biology Technology, vol. 111, pp. 352–361, 2016, doi: 10.1016/j.postharvbio.2015.09.027.
[9] Y. Lu and R. Lu, “Enhancing chlorophyll fluorescence imaging under structured illumination with automatic vignetting correction for detection of chilling injury in cucumbers,” Computers and Electronics in Agriculture, vol. 168, p. 105145, 2020, doi: 10.1016/j.compag.2019.105145.
[10] K. Luengwilai and D. M. Beckles, “Effect of low temperature storage on fruit physiology and carbohydrate accumulation in tomato ripening– inhibited mutants,” Journal of Stored Products and Postharvest Research, vol. 4, pp. 35–43, 2013, doi: 10.5897/JSPPR10.012.
[11] L. Mao, G. Wang, C. Zhu, and H. Pang, “Involvement of phospholipase D and lipoxygenase in response to chilling stress in postharvest cucumber fruits,” Plant Science, vol. 172, pp. 400–405, 2007, doi: 10.1016/j.plantsci.2006.10.002.
[12] C. Han, J. Zuo, Q. Wang, H. Dong, and L. Gao, “Salicylic acid alleviates postharvest chilling injury of sponge gourd (Luffa cylindrica),” Journal of Integrative Agriculture, vol. 16, pp. 735–741, 2017, doi: 10.1016/S2095-3119(16)61390-4.
[13] C. J. Baker and M. N. Mock, “An improved method for monitoring cell death in cell suspension and leaf disc assays using evans blue,” Plant Cell, Tissue and Organ Culture, vol. 39, pp. 7–12, 1994, doi: 10.1007/BF00037585.
[14] S. Lutts, J. M. Kinect, and J. Bouharmont, “NaClinduced senescence in leaves of rice (Oryza sativa L.) cultivars differing in salinity resistance,” Annals of Botany, vol. 78, pp. 389–398, 1996, doi: 10.1006/anbo.1996. 0134.
[15] K. S. Krishan Chaitanya and S. C. Naithani, “Role of superoxide, lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn.f.,” New Phytologist, vol. 126, pp. 623–627, 1994, doi: 10.1111/ j.14698137.1994.tb02957.x.
[16] M. Zouari, C. B. Ahmed, W. Zorrig, N. Elloumi, M. Rabhi, D. Delmail, B. B. Rouina, P. Labrousse, and F. B. Abdallah, “Exogenous proline mediates alleviation of cadmium stress by promoting photosynthetic activity, water status and antioxidative enzymes activities of young date palm (Phoenix dactylifera L.),” Ecotoxicology and Environmental Safety, vol. 128, pp. 100–108, 2016, doi: 10. 1016/j.ecoenv.2016. 02.015.
[17] S. Dipierro and S. De Leonardis, “The ascorbate system and lipid peroxidation in stored potato (Solanum tuberosum L.) tubers,” Journal of Experimental Botany, vol. 48, pp. 779–783, 1997, doi: 10.1093/jxb/48.3.779.
[18] R. S. Dhindsa, P. Plumb-Dhindsa, and T. A. Thorpe, “Leaf senescence: Correlated with increased levels of membrane permeability and lipid peroxidation, and decreased levels of superoxide dismutase and catalase,” Journal of Experimental Botany, vol. 32, pp. 93–101, 1981, doi: 10.1093/jxb/32.1.93.
[19] A. Jiménez, J. A. Hernández, L. A. del Rio, and F. Sevilla, “Evidence for the presence of the ascorbate-glutathione cycle in mitochondria and peroxisomes of pea leaves,” Plant Physiology, vol. 114, pp. 275–284, 1997, doi: 10. 1104/pp.114.1.275.
[20] D. Martins and A. M. English, “Catalase activity is stimulated by H2O2 in rich culture medium and is required for H2O2 resistance and adaptation in yeast,” Redox Biology, vol. 2, 308–313, 2014, doi: 10.1016/j.redox. 2013.12.019.
[21] H. Song, X. Gao, B. Feng, H. Dai, P. Zhang, J. Gao, P. Wang, and Y. Chai, “Leaf senescence and physiological characters in different adzuki bean (Vigna angularis) cultivars (lines),” African Journal of Agricultural Research, vol. 8, pp. 4025–4032, 2013, doi: 10. 5897/AJAR11.1827.
[22] Y. Imahori, M. Takemura, and J. Bai, “Chilling– induced oxidative stress and antioxidant responses in mume (Prunus mume) fruit during low temperature storage,” Postharvest Biology Technology, vol. 49, pp. 54–60, 2008, doi: 10.1016/ j.postharvbio.2007.10.017.
[23] B. P. Klein and A. K. Perry, “Ascorbic acid and vitamin A activity in selected vegetables from different geographical areas of the United States,” Journal of Food Science, vol. 47, pp. 941–945, 1982, doi: 10.1111/j.1365-2621.1982.tb12750.x.
[24] R. J. Bruce and C. A. West, “Elicitation of lignin biosynthesis and isoperoxidase activity by pectic fragments in suspension cultures of castor bean,” Plant Physiology, vol. 91, pp. 889–897, 1989, doi: 10.1104/pp.91.3.88.
[25] M. M. Bradford, “A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding,” Analytical Biochemistry, vol. 72, pp. 248–254, 1976, doi: 10.1016/ 0003-2697(76)90527-3.
[26] C. N. Huang, M. J. Cornejo, D. S. Bush, and R. L. Jones, “Estimating viability of plant protoplasts using double and single staining,” Protoplasma, vol. 135, pp. 80–87, 1986.
[27] P. Vijayaraghavareddy, V. Adhinarayanreddy, R. S. Vemanna, S. Sreeman, and U. Makarla, “Quantification of membrane damage/cell death using Evan’s blue staining technique,” Bio- Protocol, vol. 7, pp. 1–8, 2017, doi: 10.21769/ BioProtoc.2519.
[28] S. S. Gill and N. Tuteja, “Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants,” Plant Physiology Biochemistry, vol. 48, pp. 909–930, 2010.
[29] J. Wong-ekkabut, Z. Xu, W. Triampo, I-M. Tang, D. P. Tieleman, and L. Monticelli, “Effect of lipid peroxidation on the properties of lipid bilayers: A molecular dynamics study,” Biophysical Journal, vol. 93, pp. 4225-4236, 2007, doi: 10.1529/ biophysj.107.112565.
[30] M. S. Aghdam and S. Bodbodak, “Physiological and biochemical mechanisms regulating chilling tolerance in fruits and vegetables under postharvest salicylates and jasmonates treatments,” Scientia Horticulturae, vol. 156, pp. 73–85, 2013, doi: 10. 1016/j.scienta.2013.03.028.
[31] R. L. Heath and L. Packer, “Photo peroxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation,” Archives of Biochemistry and Biophysics, vol. 125, pp. 189–198, 1968, doi: 10. 1016/0003-9861(68)90654-1.
[32] L. Mao, H. Pang, G. Wang, and C. Zhu “Phospholipase D and lipoxygenase activity of cucumber fruit in response to chilling stress,” Postharvest Biology Technology, vol. 44, pp. 42–47, 2007, doi: 10.1016/j.postharvbio.2006. 11.009.
[33] K. Fahmy, K. Nakano, and F. Violalita, “Investigation on quantitative index of chilling injury in cucumber fruit based on the electrolyte leakage and malondialdehyde content,” International Journal on Advanced Science, Engineering and Information Technology, vol. 5, pp. 222–225, 2015, doi: 10.18517/ ijaseit.5.3.532.
[34] P. Sharma, A. B. Jha, R. S. Dubey, and M. Pessarakli, “Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions,” Journal of Botany, vol. 2012, pp. 217037, 2012, doi: 10.1155/2012/ 217037.
[35] S. Noichinda, K. Bodhipadma, C. Mahamontri, T. Narongruk, and S. Ketsa, “Light during storage prevents loss of ascorbic acid, and increases glucose and fructose levels in Chinese kale (Brassica oleracea var. alboglabra),” Postharvest Biology Technology, vol. 44, pp. 312–315, 2007, doi: 10. 1016/j.postharvbio.2006.12.006.
[36] Y. Yabuta, T. Maruta, A. Nakamura, T. Mieda, K. Yoshimura, T. Ishikawa, and S. Shigeoka, “Conversion of L-galactono-1,4-lactone to Lascorbate is regulated by the photosynthetic electron transport chain in Arabidopsis,” Bioscience, Biotechnology, and Biochemistry, vol. 72, pp. 2598–2607, 2008, doi: 10.1271/bbb.80284
[37] R. Bhardwaj, N. Handa, R. Sharma, H. Kaur, S. Kohli, V. Kumar, and P. Kaur, “Lignins and abiotic stress: An overview,” in Physiological Mechanisms and Adaptation Strategies in Plants under Changing Environment, P. Ahmad, and M. R. Wani, Eds. New York: Springer, 2014, pp. 267–296.