AJPS  Vol.11 No.6 , June 2020
Apple Peel Biochemical Changes after Foliar Application of Combined Boron and Calcium II. Photosynthetic Pigments, Total Peroxides and Photochemical Efficiency
Abstract: Understanding of the physiological effect of post-full-bloom foliar boron combined with calcium (B+Ca) on apple (Malus domestica) peel tissues is envisaged to give way to the unknown mode-of-action by which these mineral regimens suppress fruit sunburn-browning incidence in orchards. Promotion of this mineral approach among growers, as a certainly cheaper alternative to mitigate fruit sunburn-browning incidence in apple orchards necessitates clear elucidation of its mode-of-action. This study investigated peel photosynthetic pigments and total peroxides (as a measure of oxidative stress) in three apple cultivars, Cripps Pink, Golden Delicious and Granny Smith which were treated with four B+Ca treatments varying in levels of B and Ca as well as inclusion of zinc (Zn) in one treatment. Randomized complete block design experiments with five replications were conducted at commercial farms in Western Cape, South Africa. Significant (p < 0.05) treatment effect for major pigment aspects and total peroxides occurred in all cultivars, but with strong influence of cultivar and fruit age. For instance, effect of varying B, Ca and possible B+Ca duet-effect on photosynthetic pigments occurred in Cripps Pink, whereas the Zn-treatment was mainly responsible for significant treatment effects in both Golden Delicious and Granny Smith apples. Significant treatment effect for total peroxides occurred in Cripps Pink and Granny Smith, yet significant interaction effect occurred with Golden Delicious, however, these significant results did not yield meaningful peel oxidative stress differences among the treatments. Foliar treatment differences in photochemical efficiency (Fv/Fm) were not significant. The study concludes with firm evidence that foliar B+Ca treatment composition has a significant effect on apple peel photosynthetic pigments depending on cultivar, and Zn is not desirable in the formulation of these treatments.
Cite this paper: Mwije, A. , Hoffman, E. and Lötze, E. (2020) Apple Peel Biochemical Changes after Foliar Application of Combined Boron and Calcium II. Photosynthetic Pigments, Total Peroxides and Photochemical Efficiency. American Journal of Plant Sciences, 11, 939-964. doi: 10.4236/ajps.2020.116068.

[1]   Lotze, E. and Hoffman, E.W. (2014) Foliar Application of Calcium plus Boron Reduces the Incidence of Sunburn in ‘Golden Delicious’ Apple. Journal of Horticultural Science and Biotechnology, 89, 607-612.

[2]   Lotze, E., Daiber, S.H. and Midgley, S.J.E. (2017) Boron in Combination with Calcium Reduces Sunburn in Apple Fruit. Boron, 2, 123-127.

[3]   Daiber, S.H. (2017) Quantifying Changes in Tree Physiology after Amelioration to Reduce Sunburn on Apples. MSc Thesis, Stellenbosch University, Stellenbosch.

[4]   Lotze, E., Daiber, S.H. and Midgley, S.J.E. (2018) Evaluating the Efficacy of a Preharvest Combination of Calcium and Boron as Foliar Application to Reduce Sunburn on ‘Cripps Pink’ Apples. Acta Horticulture, 1217, 61-68.

[5]   Mwije, A. (2017) Pioneering a New Paradigm of Sunburn Mitigation in Apples. In: Withers, J., Ed., Bringing Science to Communities: Voices from the Field (Issue 1), A RUFORUM Publication, Kampala, 20-23.

[6]   Mwije, A. (2020) A Study of the Dynamics of Sunburn Reduction in Apple (Malus domestica) Using Foliar Applications of a Combination of Boron and Calcium. Ph.D. Thesis, Stellenbosch University, South Africa.

[7]   Mwije, A., Hoffman, E.W. and Lotze, E. (2020) Apple Peel Biochemical Changes after Foliar Application of Boron Combined with Calcium I. Phenolics and Physico-Chemical Attributes. American Journal of Plant Sciences, 11, 965-986.

[8]   Felicetti, D.A. and Schrader, L.E. (2009) Changes in Pigment Concentrations Associated With Sunburn Browning of Five Apple Cultivars. II. Phenolics. Plant Science, 176, 84-89.

[9]   Felicetti, D.A. and Schrader, L.E. (2009) Changes in Pigment Concentrations Associated With Sunburn Browning of Five Apple Cultivars. I. Chlorophylls and Carotenoids. Plant Science, 176, 78-83.

[10]   Wünsche, J.N., Greer, D.H., Palmer, J.W., Lang, A. and McGhie, T. (2001) Sunburn—The Cost of a High Light Environment. Acta Horticulturae, 557, 349-356.

[11]   Wünsche, J.N., Lombardini, L. and Greer, D.H. (2004) “Surround” Particle Film Applications—Effects on Whole Canopy Physiology of Apple. Acta Horticulturae 636, 565-571.

[12]   Schrader, L., Sun, J., Zhang, J., Felicetti, D. and Tian, J. (2008) Heat and Light-Induced Apple Skin Disorders: Causes and Prevention. Acta Horticulturae, 772, 51-58.

[13]   Vrettos, J.S., Limburg, J. and Brudvig, G.W. (2001) Mechanism of Photosynthetic Water Oxidation: Combining Biophysical Studies of Photosystem II with Inorganic Model Chemistry. Biochimica et Biophysica Acta, 1503, 229-245.

[14]   Yachandra, V.K. and Yano, J. (2011) Calcium in the Oxygen-Evolving Complex: Structural and Mechanistic Role Determined by X-Ray Spectroscopy. Journal of Photochemistry and Photobiology B: Biology, 104, 51-59.

[15]   Yang, S., Wang, F., Guo, F., Meng, J.J., Li, X.G. and Wan, S.B. (2015) Calcium Contributes to Photoprotection and Repair of Photosystem II in Peanut Leaves during Heat and High Irradiance. Journal of Integrative Plant Biology, 57, 486-495.

[16]   Jiang, Y. and Huang, B. (2001) Effects of Calcium on Antioxidant Activities and Water Relations Associated with Heat Tolerance in Two Cool-Season Grasses. Journal of Experimental Botany, 52, 341-349.

[17]   Seth, K. and Aery, N.C. (2014) Effect of Boron on the Contents of Chlorophyll, Carotenoid, Phenol and Soluble Leaf Protein in Mung Bean, Vigna radiata (L.) Wilczek. Proceedings of National Academy of Sciences, India Section B: Biological Sciences, 84, 713-719.

[18]   Ganie, M.A., Akhter, F., Bhat, M.A., Malik, A.R., Junaid, J.M., Shah, M.A., Bhat, A.H. and Bhat, T.A. (2013) Boron—A Critical Nutrient Element for Plant Growth and Productivity with Reference to Temperate Fruits. Current Science, 104, 76-85.

[19]   Kobayashi, M., Nakagawa, H., Asaka, T. and Matoh, T. (1999) Borate Rhamnogalacturonan II Bonding Reinforced by Ca2+ Retains Pectic Polysaccharides in Higher-Plant Cell Walls. Plant Physiology, 119, 199-204.

[20]   Bolanos, L., Lukaszewski, K., Bonilla, I. and Blevins, D. (2004) Why Boron? Plant Physiology and Biochemistry, 42, 907-912.

[21]   Camacho-Cristobal, J.J., Herrera-Rodriguez, M.B., Beato, V.M., Rexach, J., Navarro-Gochicoa, M.T., Maldonado, J.M. and Gonzalez-Fontes, A. (2008) The Expression of Several Cell Wall-Related Genes in Arabidopsis Roots is Down-Regulated under Boron Deficiency. Environmental and Experimental Botany, 63, 351-358.

[22]   Verma, S. and Dubey, R.S. (2003) Lead Toxicity Induces Lipid Peroxidation and Alters the Activities of Antioxidant Enzymes in Growing Rice Plants. Plant Science, 164, 645-655.

[23]   Skorzynska-Polit, E. 2007. Lipid Peroxidation in Plant Cells, Its Physiological Role and Changes under Heavy Metal Stress. Acta Societatis Botanicorum Poloniae, 76, 49-54.

[24]   Xu, S., Li, J., Zhang, X., Wei, H. and Cui, L. (2006) Effects of Heat Acclimation Pretreatment on Changes of Membrane Lipid Peroxidation, Antioxidant Metabolites, and Ultrastructure of Chloroplasts in Two Cool-Season Turfgrass Species under Heat Stress. Environmental and Experimental Botany, 56, 274-285.

[25]   Jiang, Y. and Huang, B. (2001) Drought and Heat Stress Injury to Two Cool-Season Turfgrasses in Relation to Antioxidant Metabolism and Lipid Peroxidation. Crop Science, 41, 436-442.

[26]   Song, X., Wang, Y. and Lv, X. (2016) Responses of Plant Biomass, Photosynthesis and Lipid Peroxidation to Warming and Precipitation Change in Two Dominant Species (Stipa grandis and Leymus chinensis) from North China Grasslands. Ecology and Evolution, 6, 1871-1882.

[27]   Agarwal, S., Sairam, R.K., Srivastava, G.C., Tyagi, A. and Meena, R.C. (2005) Role of ABA, Salicylic Acid, Calcium and Hydrogen Peroxide on Antioxidant Enzymes Induction in Wheat Seedlings. Plant Science, 169, 559-570.

[28]   Gill, S.S. and Tuteja, N. (2010) Reactive Oxygen Species and Antioxidant Machinery in Abiotic Stress Tolerance in Crop Plants. Plant Physiology and Biochemistry, 48, 909-930.

[29]   Karuppanapandian, T., Moon, J.C., Kim, C., Manoharan, K. and Kim, W. (2011) Reactive Oxygen Species in Plants: Their Generation, Signal Transduction, and Scavenging Mechanisms. Australian Journal of Crop Science, 5, 709-725.

[30]   Chen, L.S., Li, P. and Cheng, L. (2008) Effects of High Temperature Coupled with High Light on the Balance between Photooxidation and Photoprotection in the Sun-Exposed Peel of Apple. Planta, 228, Article No.: 745.

[31]   Chen, L.-S., Li, P. and Cheng, L. (2009) Comparison of Thermotolerance of Sun-Exposed Peel and Shaded Peel of “Fuji” Apple. Environmental and Experimental Botany, 66, 110-116.

[32]   Yuri, J.A., Neira, A., Quilodran, A., Razmilic, I., Motomura, Y., Torres, C. and Palomo, I. (2010) Sunburn on Apples is Associated with Increases in Phenolic Compounds and Antioxidant Activity as a Function of the Cultivar and Areas of the Fruit. Journal of Food, Agriculture and Environment, 8, 920-925.

[33]   Yuri, J.A., Neira, A., Maldonado, F., Quilodran, A., Simeone, D., Razmilic, I. and Palomo, I. (2014) Total Phenol and Quercetin Content and Antioxidant Activity in Apples in Response to Thermal, Light Stress and to Organic Management. Journal of Applied Botany and Food Quality, 87, 131-138.

[34]   Zhang, J., Niu, J., Duan, Y., Zhang, M., Liu, J., Li, P. and Ma, F. (2015) Photoprotection Mechanism in the “Fuji” Apple Peel at Different Levels of Photooxidative Sunburn. Physiologia Plantarum, 154, 54-65.

[35]   Policarpo, M., Di Marco, L., Farina, V. and Tagliavini, S. (2002) Effect of Foliar Nutrition on Peach (Prunus persica L. Batsch) Yield and Fruit Quality as Related to Different Crop Loads. Acta Horticulturae, 594, 659-666.

[36]   Garc, M.F., Hern, J.A., Lopez-Gomez, E., San Juan, M.A., Diaz-Vivancos, P., Mataix Beneyto, J., Garcia-Legaz, M.F. and Hernandez, J.A. (2007) Effect of Rootstocks Grafting and Boron on the Antioxidant Systems and Salinity Tolerance of Loquat Plants (Eriobotrya japonica Lindl.). Environmental and Experimental Botany, 60, 151-158.

[37]   Thurzo, S., Szabo, Z., Nyeki, J., Nagy, P.T., Silva, A.P. and Goncalves, B. (2010) Effect of Boron and Calcium Sprays on Photosynthetic Pigments, Total Phenols and Flavonoid Content of Sweet Cherry (Prunus avium L.). Acta Horticulturae, 868, 457-462.

[38]   Singh, D.P., Beloy, J., Mcinerney, J.K. and Day, L. (2012) Impact of Boron, Calcium and Genetic Factors on Vitamin C, Carotenoids, Phenolic Acids, Anthocyanins and Antioxidant Capacity of Carrots (Daucus carota). Food Chemistry, 132, 1161-1170.

[39]   Sakhonwasee, S. and Phingkasan, W. (2017) Effects of the Foliar Application of Calcium on Photosynthesis, Reactive Oxygen Species Production, and Changes in Water Relations in Tomato Seedlings under Heat Stress. Horticulture Environment and Biotechnology, 58, 119-126.

[40]   Lichtenthaler, H.K. (1987) Chlorophylls and Carotenoids: Pigments of Photosynthetic Biomembranes. Methods in Enzymology, 148, 350-382.

[41]   Lichtenthaler, H.K. and Buschmann, C. (2001) Chlorophylls and Carotenoids: Measurement and Characterization by UV-VIS Spectroscopy. Current Protocols in Food Analytical Chemistry, 1, F4.3.1-F4.3.8.

[42]   Brennan, T. and Frenkel, C. (1977) Involvement of Hydrogen Peroxide in the Regulation of Senescence in Pear. Plant Physiology, 59, 411-416.

[43]   Du, Z. and Bramlage, W.J. (1995) Peroxidative Activity of Apple Peel in Relation to Development of Poststorage Disorders. HortScience, 30, 205-209.

[44]   Statistica Software (2019).

[45]   Piskolczi, M., Varga, C. and Racskó, J. (2004) A Review of the Meteorological Causes of Sunburn Injury on the Surface of Apple Fruit (Malus domestica Borkh). Journal of Fruit and Ornamental Plant Research, 12, 245-252.

[46]   Mainla, L., Moor, U., Karp, K. and Pussa, T. (2011) The Effect of Genotype and Rootstock on Polyphenol Composition of Selected Apple Cultivars in Estonia. Zemdirbyste-Agriculture, 98, 63-70.

[47]   Kviklys, D., Liaudanskas, M., Janulis, V., Viskelis, P., Rubinskiene, M., Lanauskas, J. and Uselis, N. (2014) Rootstock Genotype Determines Phenol Content in Apple Fruits. Plant, Soil and Environment, 60, 234-240.

[48]   Feng, F., Li, M., Ma, F. and Cheng, L. (2014) The Effects of Bagging and Debagging on External Fruit Quality, Metabolites, and the Expression of Anthocyanin Biosynthetic Genes in “Jonagold” Apple (Malus domestica Borkh.). Scientia Horticulturae, 165, 123-131.

[49]   Feng, F., Li, M., Ma, F. and Cheng, L. (2014) Effects of Location Within the Tree Canopy on Carbohydrates, Organic Acids, Amino Acids and Phenolic Compounds in the Fruit Peel and Flesh from Three Apple (Malus × domestica) Cultivars. Horticulture Research, 1, Article No.: 14019.

[50]   De Paepe, D., Valkenborg, D., Noten, B., Servaes, K., Diels, L., De Loose, M., Van Droogenbroeck, B. and Voorspoels, S. (2015) Variability of the Phenolic Profiles in the Fruits From Old, Recent and New Apple Cultivars Cultivated in Belgium. Metabolomics, 11, 739-752.

[51]   Le Bourvellec, C., Bureau, S., Renard, C.M.G.C., Plenet, D., Gautier, H., Touloumet, L., Girard, T. and Simon, S. (2015) Cultivar and Year Rather than Agricultural Practices Affect Primary and Secondary Metabolites in Apple Fruit. PLoS ONE, 10, e0141916.

[52]   Bian, W., Barsan, C., Egea, I., Purgatto, E., Chervin, C., Zouine, M., Latche, A., Bouzayen, M. and Pech, J.C. (2011) Metabolic and Molecular Events Occurring During Chromoplast Biogenesis. Journal of Botany, 2011, Article ID: 289859.

[53]   Egea, I., Bian, W., Barsan, C., Jauneau, A., Pech, J.C., Latche, A., Li, Z. and Chervin, C. (2011) Chloroplast to Chromoplast Transition in Tomato Fruit: Spectral Confocal Microscopy Analyses of Carotenoids and Chlorophylls in Isolated Plastids and Time-Lapse Recording on Intact Live Tissue. Annals of Botany, 108, 291-297.

[54]   Delgado-Pelayo, R., Gallardo-Guerrero, L. and Hornero-Mendez, D. (2014) Chlorophyll and Carotenoid Pigments in the Peel and Flesh of Commercial Apple Fruit Varieties. Food Research International, 65, 272-281.

[55]   Merzlyak, M.N. (2006) Modeling Pigment Contributions to Spectral Reflection of Apple Fruit. Photochemical & Photobiological Sciences, 5, 748-754.

[56]   Kim, E.H., Li, X.P., Razeghifard, R., Anderson, J.M., Niyogi, K.K., Pogson, B.J. and Chow, W.S. (2009) The Multiple Roles of Light-Harvesting Chlorophyll a/b-Protein Complexes Define Structure and Optimize Function of Arabidopsis Chloroplasts: A Study Using Two Chlorophyll b-Less Mutants. Biochimica et Biophysica Acta, 1787, 973-984.

[57]   Hortensteiner, S. and Krautler, B. (2011) Chlorophyll Breakdown in Higher Plants. Biochimica et Biophysica Acta, 1807, 977-988.

[58]   Tanaka, R. and Tanaka, A. (2011) Chlorophyll Cycle Regulates the Construction and Destruction of the Light-Harvesting Complexes. Biochimica et Biophysica Acta, 1807, 968-976.

[59]   Hannoufa, A. and Hossain, Z. (2012) Regulation of Carotenoid Accumulation in Plants. Biocatalysis and Agricultural Biotechnology, 1, 198-202.

[60]   Havaux, M. (1998) Carotenoids as Membrane Stabilizers in Chloroplasts. Trends in Plant Science, 3, 147-151.

[61]   Ampomah-Dwamena, C., Dejnoprat, S., Lewis, D., Sutherland, P., Volz, R.K. and Allan, A.C. (2012) Metabolic and Gene Expression Apple (Malus × domestica) Carotenogenesis. Journal of Experimental Botany, 63, 4497-4511.

[62]   Racchi, M.L. (2013) Antioxidant Defenses in Plants with Attention to Prunus and Citrus spp. Antioxidants, 2, 340-369.

[63]   Bandurska, H., Niedziela, J. and Chadzinikolau, T. (2013) Separate and Combined Responses to Water Deficit and UV-B Radiation. Plant Science, 213, 98-105.

[64]   Nisar, N., Li, L., Lu, S., Khin, N.C. and Pogson, B.J. (2015) Carotenoid Metabolism in Plants. Molecular Plant, 8, 68-82.

[65]   Merzlyak, M.N. and Solovchenko, A.E. (2002) Photostability of Pigments in Ripening Apple Fruit: A Possible Photoprotective Role of Carotenoids during Plant Senescence. Plant Science, 163, 881-888.

[66]   Merzlyak, M.N., Solovchenko, A.E. and Chivkunova, O.B. (2002) Patterns of Pigment Changes in Apple Fruits during Adaptation to High Sunlight and Sunscald Development. Plant Physiology and Biochemistry, 40, 679-684.

[67]   Felicetti, D.A. and Schrader, L.E. (2008) Changes in Pigment Concentrations Associated with the Degree of Sunburn Browning of “Fuji” Apple. Journal of the American Society of Horticultural Science, 133, 27-34.

[68]   Cripps, J.E.L., Richards, L.A. and Mairata, A.M. (1993) “Pink Lady” Apple. HortScience, 28, 1057.

[69]   Charoenchongsuk, N., Ikeda, K., Itai, A., Oikawa, A. and Murayama, H. (2015) Comparison of the Expression of Chlorophyll-Degradation-Related Genes During Ripening Between Stay-Green and Yellow-Pear Cultivars. Scientia Horticulturae, 181, 89-94.

[70]   Agati, G., Azzarello, E., Pollastri, S. and Tattini, M. (2012) Flavonoids as Antioxidants in Plants: Location and Functional Significance. Plant Science, 196, 67-76.

[71]   Agati, G., Brunetti, C., Ferdinando, M.D., Ferrini, F., Pollastri, S. and Tattini, M. (2013) Functional Roles of Flavonoids in Photoprotection: New Evidence, Lessons from the Past. Plant Physiology and Biochemistry, 72, 35-45.

[72]   Dellapenna, D. (1999) Carotenoid Synthesis and Function in Plants: Insights from Mutant Studies in Arabidopsis. Pure and Applied Chemistry, 71, 2205-2212.

[73]   Havaux, M. and Niyogi, K.K. (1999) The Violaxanthin Cycle Protects Plants from Photooxidative Damage by More Than One Mechanism. Proceedings of the National Academy of Sciences of the United States of America, 96, 8762-8767.

[74]   Mu, P., Li, X.P. and Niyogi, K.K. (2001) Update on Photosynthesis Non Photochemical Quenching. A Response to Excess Light Energy. Plant Physiology, 125, 1558-1566.

[75]   Ritchie, G.A. (2006) Chlorophyll Fluorescence: What Is It and What Do the Numbers Mean? National Proceedings: Forest and Conservation Nursery Associations, RMRS-P-43, 34–43.

[76]   Dussi, M.C., Giardina, G. and Reeb, P. (2005) Shade Nets Effect on Canopy Light Distribution and Quality of Fruit and Spur Leaf on Apple cv. Fuji. Spanish Journal of Agricultural Research, 3, 253-260.

[77]   Fan, L., Song, J., Forney, C.F. and Jordan, M.A. (2011) Fruit Maturity Affects the Response of Apples to Heat Stress. Postharvest Biology and Technology, 62, 35-42.

[78]   Racskó, J. and Schrader, L.E. (2012) Sunburn of Apple Fruit: Historical Background, Recent Advances and Future Perspectives. Critical Reviews in Plant Sciences, 31, 455-504.

[79]   Rao, M. V, Watkins, C.B., Brown, S.K. and Weeden, N.F. (1998) Active Oxygen Species Metabolism in “White Angel” × “Rome Beauty” Apple Selections Resistant and Susceptible to Superficial Scald. Journal of the American Society for Horticultural Science, 123, 299-304.

[80]   Blokhina, O., Virolainen, E. and Fagerstedt, K.V. (2003) Antioxidants, Oxidative Damage and Oxygen Deprivation Stress: A Review. Annals of Botany, 91, 179-194.

[81]   Schrader, L.E., Zhang, J. and Duplaga, W.K. (2001) Two Types of Sunburn in Apple Caused by High Fruit Surface (Peel) Temperature. Plant Health Progress, 2, No. 1.

[82]   Wolfe, K., Wu, X. and Liu, R.H. (2003) Antioxidant Activity of Apple Peels. Journal of Agricultural and Food Chemistry, 51, 609-614.

[83]   Tsao, R., Yang, R., Xie, S., Sockovie, E. and Khanizadeh, S. (2005) Which Polyphenolic Compounds Contribute to the Total Antioxidant Activities of Apple? Journal of Agricultural and Food Chemistry, 53, 4989-4995.

[84]   Moyle, C.W.A. (2011) Polyphenols in Apples and Their Interactions with Vascular Endothelial Cells. PhD Dissertation, University of East Anglia, Norwich.

[85]   Kalinowska, M., Bielawska, A., Lewandowska-Siwkiewicz, H., Priebe, W. and Lewandowski, W. (2014) Apples: Content of Phenolic Compounds vs. Variety, Part of Apple and Cultivation Model, Extraction of Phenolic Compounds, Biological Properties. Plant Physiology and Biochemistry, 84, 169-188.

[86]   Perez, F.J. and Rubio, S. (2006) An Improved Chemiluminescence Method for Hydrogen Peroxide Determination in Plant Tissues. Plant Growth Regulation, 48, 89-95.

[87]   Du, Z. and Bramlage, W.J. (1992) Modified Thiobarbituric Acid Assay for Measuring Lipid Oxidation in Sugar-Rich Plant Tissue Extracts. Journal of Agricultural and Food Chemistry, 40, 1566-1570.

[88]   Mishra, R.K. and Singhal, G.S. (1992) Function of Photosynthetic Apparatus of Intact Wheat Leaves under High Light and Heat Stress and its Relationship with Peroxidation of Thylakoid Lipids. Plant Physiology, 98, 1-6.

[89]   Vilaplana, R., Valentines, M.C., Toivonen, P. and Larrigaudiere, C. (2006) Antioxidant Potential and Peroxidative State of “Golden Smoothee” Apples Treated with 1-Methylcyclopropene. Journal of the American Society for Horticultural Science, 131, 104-109.

[90]   Duan, X., Liu, T., Zhang, D., Su, X., Lin, H. and Jiang, Y. (2011) Effect of Pure Oxygen Atmosphere on Antioxidant Enzyme and Antioxidant Activity of Harvested Litchi Fruit during Storage. Food Research International, 44, 1905-1911.

[91]   Bakhshi, D. and Arakawa, O. (2006) Induction of Phenolic Compounds Biosynthesis with Light Irradiation in the Flesh of Red and Yellow Apples. Journal of Applied Horticulture, 8, 101-104.

[92]   Jakopic, J., Stampar, F. and Veberic, R. (2009) The Influence of Exposure to Light on the Phenolic Content of ‘Fuji’ Apple. Scientia Horticulturae, 123, 234-239.

[93]   Hodges, D.M., Delong, J.M., Forney, C.F. and Prange, R.K. (2015) Improving the Thiobarbituric Acid-Reactive-Substances Assay for Estimating Lipid Peroxidation in Plant Tissues Containing Anthocyanin and Other Interfering Compounds. Planta, 207, 604-611.

[94]   Macarisin, D., Cohen, L., Eick, A., Rafael, G., Belausov, E., Wisniewski, M. and Droby, S. (2007) Penicillium digitatum Suppresses Production of Hydrogen Peroxide in Host Tissue during Infection of Citrus Fruit. Postharvest Pathology and Mycotoxins, 97, 1491-1500.

[95]   Sabban-Amin, R., Feygenberg, O., Belausov, E. and Pesis, E. (2011) Low Oxygen and 1-MCP Pretreatments Delay Superficial Scald Development by Reducing Reactive Oxygen Species (ROS) Accumulation in Stored ‘Granny Smith’ Apples. Postharvest Biology and Technology, 62, 295-304.

[96]   Mditshwa, A., Fawole, O.A., Vries, F., van Der Merwe, K., Crouch, E. and Opara, U.L. (2016) Classification of ‘Granny Smith’ Apples with Different Levels of Superficial Scald Severity Based on Targeted Metabolites and Discriminant Analysis. Journal of Applied Botany and Food Quality, 89, 49-55.

[97]   Kong, W., Liu, F., Zhang, C., Zhang, J. and Feng, H. (2016) Non-Destructive Determination of Malondialdehyde (MDA) Distribution in Oilseed Rape Leaves by Laboratory Scale NIR Hyperspectral Imaging. Scientific Reports, 6, Article No.: 35393.

[98]   Axelrod, B., Cheesbrough, T.M. and Laakso, S. (1981) Lipoxygenase from Soybeans: EC Linoleate: Oxygen Oxidoreductase. Methods in Enzymology, 71, 441-451.

[99]   Dix, T.A. and Aikens, J. (1993) Mechanisms and Biological Relevance of Lipid Peroxidation Initiation. Chemical Research in Toxicology, 6, 2-18.

[100]   Lynch, D.V. and Thompson, J.E. (1984) Lipoxygenase-Mediated Production of Superoxide Anion in Senescing Plant Tissue. FEBS Letters, 173, 251-254.

[101]   He, Y., Fukushige, H., Hildebrand, D.F. and Gan, S. (2002) Evidence Supporting a Role of Jasmonic Acid in Arabidopsis Leaf Senescence. Plant Physiology, 128, 435-441.

[102]   Berger, S., Weichert, H., Porzel, A., Wasternack, C., Kuhn, H. and Feussner, I. (2001) Enzymatic and Non-Enzymatic Lipid Peroxidation in Leaf Development. Biochimica et Biophysica Acta, 1533, 266-276.

[103]   Spiteller, G. (2003) The Relationship Between Changes in the Cell Wall, Lipid Peroxidation, Proliferation, Senescence and Cell Death. Physiologia Plantarum, 119, 5-18.

[104]   Bi, X., Zhang, J., Chen, C., Zhang, D., Li, P. and Ma, F. (2014) Anthocyanin Contributes more to Hydrogen Peroxide Scavenging than Other Phenolics in Apple Peel. Food Chemistry, 152, 205-209.

[105]   Zhang, J., Chen, C., Zhang, D., Li, H., Li, P. and Ma, F. (2014) Reactive Oxygen Species Produced via Plasma Membrane NADPH Oxidase Regulate Anthocyanin Synthesis in Apple Peel. Planta, 240, 1023-1035.

[106]   Lata, B., Trampczyńska, A. and Oles, M. (2005) Antioxidant Content in the Fruit Peel, Flesh and Seeds of Selected Apple Cultivars during Cold Storage. Folia Horticulturae, 17, 47-60.

[107]   Solovchenko, A. and Schmitz-Eiberger, M. (2003) Significance of Skin Flavonoids for UV-B-Protection in Apple Fruits. Journal of Experimental Botany, 54, 1977-1984.