Sun-related physiological disorders have a substantial annual economic impact on the worldwide apple (M. domestica) industry, particularly when grown in semiarid climates where losses can be from 10% to 50% of total production (Racsko and Schrader, 2012; Yuri et al., 2000b). Climatic conditions in these regions can elevate photooxidative and heat stress throughout the growing season affecting the tree and fruit physiology. Skin browning or “stain” can develop on ‘Fuji’ apples during cold storage (Mattheis, 1996; Schrader et al., 2008). “Stain” symptoms are typically browning or discoloration that begin to appear 1–2 months after harvest (Schrader et al., 2008) on the periphery of sunburned or sun-exposed areas of the peel (Felicetti and Schrader, 2010; Kupferman, 1994). Symptoms are very superficial and only occur in the first epidermal cell layer of the peel. To date, there are no known postharvest crop protectant or storage regimes that reduce this problem. “Stain” is not prevented by postharvest diphenylamine or AsA (0.2%) treatments at harvest (Kupferman, 1994).
As with sunscald of ‘Granny Smith’ apples (Contreras et al., 2008; Hernandez et al., 2014; Lurie et al., 1991), “stain” development is associated with sun exposure in the orchard as well as sunburn incidence and severity (Fan and Mattheis, 1998; Felicetti and Schrader, 2010; Schrader et al., 2003, 2008). Fuji apples are highly susceptible to “stain,” although it can occur on other cultivars including Royal Gala and Honeycrisp apples. Limiting sunlight exposure on ‘Fuji’ apples using bags prevents “stain” development (Fan and Mattheis, 1998). Raynox® is an orchard-applied carnauba-based coating that blocks ultraviolet-B and, consequently, reduces sunburn and “stain” incidence (Schrader et al., 2008).
Sun injury or sunburn of fleshy fruit is caused by absorption of excess solar energy by exposed tissue, leading to photoinhibition and oxidative stress (Ma and Cheng, 2003; 2004; Torres et al., 2006). Defense mechanisms activated in tissue exposed to direct sunlight or during early stages of sunburn include antioxidants (i.e., AsA, GSH) and enzymes functioning as antioxidants or regeneration of antioxidants such as, ascorbate peroxidase (APX; EC 184.108.40.206), dehydroascorbate reductase (DHAR; EC 220.127.116.11), monodehydroascorbate reductase (MDHAR; EC 18.104.22.168), glutathione reductase (GR; EC 22.214.171.124), catalase (CAT; EC 126.96.36.199), and superoxide dismutase (EC 188.8.131.52) (Chen et al., 2008; Ma and Cheng, 2003, 2004). However, activity of these recycling enzymes is not always higher in sun-damaged apple peel (Zhang et al., 2014).
Levels of certain pigments, including chlorophylls and carotenoids, decrease as sun-injury symptoms increase, whereas others, including xanthophylls, increase with light stress, possibly as a photoprotective mechanism (Chen et al., 2008; Ma and Cheng, 2003; Tartachnyk et al., 2012; Torres et al., 2006; Wünsche et al., 2001). Phenolic compounds rapidly accumulate on sun-exposed peel in response to direct sunlight (Felicetti and Schrader, 2008; Yuri et al., 2010). Phenolic compounds also appear to be directly involved in sunscald development in ‘Granny Smith’ apples during cold storage (Hernandez et al., 2014). The antioxidative capacity and regeneration of ascorbate by the AsA–GSH pathway ostensibly has an indirect role in sunscald development by improving defense against postharvest oxidative stresses (Hernandez et al., 2014). During this process, quercetin oxidation and accumulation of its brown products may be responsible for the symptoms (Jimenez and Garcia-Carmona, 1999). Flavonols, including quercetin can be substrates for polyphenol oxidase from a variety of plant species (Gasic et al., 2004; Jimenez and Garcia-Carmona, 1999) indicating that this defense-related process may, likewise, have a similar function in apple in this instance. We hypothesize that, while mechanisms resulting in sunscald may be similar, they can culminate in different symptoms on ‘Fuji’ peel. Accordingly, our objective was to evaluate antioxidant metabolism to compare “stain” and sunscald development.
Chen, L-S., Li, P. & 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 228 745 756
Contreras, C., Zoffoli, J.P., Alcalde, J.A. & Ayala, M. 2008 Evolution of sunburn damage on ‘Granny Smith’ apples during storage Cien. Inv. Agr. 35 113 122
Davey, M.W., Auewerkerken, A. & Keulemans, J. 2007 Relationship of apple vitamin C and antioxidant contents to harvest date and postharvest pathogen infection J. Sci. Food Agr. 87 802 813
Fan, X. & Mattheis, J. 1998 Bagging ‘Fuji’ apples during fruit development affects color development and storage quality HortScience 33 1235 1238
Felicetti, D.A. & Schrader, L.E. 2008 Changes in pigment concentrations associated with the degree of sunburn browning of ‘Fuji’ apple J. Amer. Soc. Hort. Sci. 133 27 34
Felicetti, D.A. & Schrader, L.E. 2009a Changes in pigment concentrations associated with sunburn browning of five apple cultivars. I. Chlorophylls and carotenoids Plant Sci. 176 78 83
Felicetti, D.A. & Schrader, L.E. 2009b Changes in pigment concentrations associated with sunburn browning of five apple cultivars. II. Phenolics Plant Sci. 176 84 89
Felicetti, D.A. & Schrader, L.E. 2010 Postharvest changes in pigment concentrations in ‘Fuji’ apples with ‘Fuji’ stain Scientia Hort. 125 283 288
Felicetti, E. & Mattheis, J.P. 2010 Quantification and histochemical localization of ascorbic acid in ‘Delicious’, ‘Golden Delicious’, and ‘Fuji’ apple fruit during on-tree development and cold storage Postharvest Biol. Technol. 56 56 63
Gasic, K., Hernandez, A. & Korban, S.S. 2004 RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction Plant Mol. Biol. Rpt. 22 437
Hernandez, O., Torres, C., Moya-León, M., Opazo, M. & Razmilic, I. 2014 Roles of the ascorbate-glutathione cycle, pigments and phenolics in postharvest ‘sunscald’ development on ‘Granny Smith’ apples (Malus domestica Borkh.) Postharvest Biol. Technol. 87 79 87
Li, M., Ma, F., Zhang, M. & Pu, F. 2008 Distribution and metabolism of ascorbic acid in apple fruits (Malus domestica Borkh cv. Gala) Plant Sci. 174 606 612
Lichtenthaler, H.K. & Wellburn, A.R. 1983 Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents Biochem. Soc. Trans. 603 591 592
Lurie, S., Pesis, E. & Ben-Arie, R. 1991 Darkening of sunscald on apples in storage is a non-enzymatic and non-oxidative process Postharvest Biol. Technol. 1 119 125
Ma, F. & Cheng, L. 2003 The sun-exposed peel of apple fruit has higher xanthophyll cycle-dependent thermal dissipation and antioxidants of the ascorbate-glutathione pathway than the shaded peel Plant Sci. 165 819 827
Ma, F. & Cheng, L. 2004 Exposure of the shaded side of apple fruit to full sun leads to up-regulation of both the xanthophylls cycle and the ascorbate-glutathione cycle Plant Sci. 166 1479 1486
Merzlyak, M.N. & Solovchenko, A. 2002a Photostability of pigments in ripening apple fruit: A possible photoprotective role of carotenoids during plant senescence Plant Sci. 136 881 888
Merzlyak, M.N., Solovchenko, A. & Chivkunova, O.B. 2002b Patterns of pigment changes in apple fruits during adaptation to high sunlight and sunscald development Plant Physiol. Biochem. 40 679 684
Racsko, J. & Schrader, L.E. 2012 Sunburn of apple fruit: Historical background, recent advances and future perspectives Crit. Rev. Plant Sci. 31 6 455 504
Schrader, L., Sun, J., Felicetti, D., Seo, J., Jedlow, L. & Zhang, J. 2003 Stress-induced disorders: Effects on apple fruit quality. Washington Tree Fruit Postharvest Conference. p. 1–7
Schrader, L., Sun, J., Zhang, J., Seo, J., Jedlow, L. & Felicetti, D. 2004 Fruit skin disorders. Washington Tree Fruit Postharvest Conference. p. 1–4
Schrader, L.E., Sun, J., Zhang, J., Felicetti, D. & Tian, J. 2008 Heat and light-induced apple skin disorders: Causes and prevention Acta Hort. 772 51 58
Tartachnyk, I., Kuckenberg, J., Yuri, J.A. & Noga, G. 2012 Identifying fruit characteristics for non-invasive detection of sunburn in apple Scientia Hort. 134 108 113
Torres, C.A., Andrews, P.K. & Davies, N.M. 2006 Physiological and biochemical responses of fruit exocarp of tomato (Lycopersicum esculentum Mill.) mutants to natural photo-oxidative conditions J. Expt. Bot. 57 1933 1947
Van der Sluis, A., Dekker, M., Jager, A. & Jongen, W. 2001 Activity and concentration of polyphenolic antioxidants in apple: Effect of cultivar, harvest year, and storage conditions J. Agr. Food Chem. 49 3606 3613
Yuri, J.A., Neira, A., Quilodran, A., Razmilic, I., Motomura, Y., Torres, C. & 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 J. Food Agr. Environ. 8 920 925
Yuri, J.A., Torres, C. & Vásquez, J.L. 2000b Sunburn on apples. I Damage evaluation and control methods Agrociencia 16 1 13 21 (In Spanish with English summary)
Zhang, J., Niu, J., Duan, Y., Zhang, M., Liu, J., Li, P. & Ma, F. 2014 Photoprotection mechanism in the ‘Fuji’ apple peel at different levels of photooxidative sunburn Physiol. Plant. 154 54 65
Zubini, P., Baraldi, E., De Santis, A., Bertolini, P. & Mari, M. 2007 Expression of anti-oxidant enzyme genes in scald-resistant ‘Belfort’ and scald-susceptible ‘Granny Smith’ apples during cold storage J. Hort. Sci. Biotechnol. 82 149 155