A convergence of sunlight and cold chain: The influence of sun exposure on postharvest apple peel metabolism

Highlights

• Sunlight exposure continues to alter apple appearance during cold storage.

• Metabolism linked with sun stress continues during storage.

• Metabolism related to ripening and quality is different during storage.

• Sorting based on cumulative sun exposure may be possible using these metabolic targets.

Abstract

Excess solar irradiation is responsible for commercially significant annual losses of apple fruit, and those losses are expected to increase in the majority of the world’s apple production regions. Losses are not limited to the orchard but are also represented by disorders that develop in the cold chain such as sunscald and elevated lenticel damage. Similarly, metabolism during storage would reflect changes and even diverge during ripening and cold storage depending upon relative amount of light exposure in the orchard. To determine and track these changes alongside changes of appearance, ‘September Wonder Fuji’, ‘Gala’, ‘Granny Smith’, and ‘Honeycrisp’ apples were selected from the periphery on the south-facing side of trees for contrasting sun exposure on opposite aspects, stored in 1 °C air, and peel from opposing sides sampled sequentially from 0 to 6 months. Additional sunburned peel was sampled at 0 and 6 months. Sun exposure provoked broad relative responses from multiple pathways indicative of solar stress response. Responses include accumulation of well-characterized photoprotective responses including accumulation of flavonol glycoside and carotenoid, compatible solutes, and primary metabolites. Others include previously unreported or lesser understood responses such as those potentially impacting membrane properties (including changes in levels of monogalactosyldiacyglycerides and stigmasteryl glycosides), epicuticular surface metabolites (including pentacyclic triterpenes and diacylglycerides), and production of volatile alkenals indicative of residual solar stress during storage. Taken together, metabolic evidence indicates orchard light environment continues to impact not only appearance, but also rate of ripening and potentially fruit quality, even on the same apple. In this way, light exposure of any given apple could influence every cold chain management decision, and sorting apples at-harvest according to cumulative light exposure would improve apple consistency while potentially avoiding losses due to peel disorders.

Introduction

Adequate levels of high quality sunlight are critical to apple production. Fruit growth and red peel color development is optimal under diffuse light and relatively moderate temperatures (Saure, 1990). However, exposure of unacclimated apples to direct sunlight, especially at high ambient orchard temperatures, can adversely impact appearance leading to immediate injury in the form of sunburn necrosis, sunburn browning, and photooxidative sunburn as well as postharvest disorders including delayed sunscald, lenticel blotch, and stain (Racsko and Schrader, 2012). In fact, disorders related to high sunlight continue to be principal sources of annual apple crop loss reaching approximately 10–25 % in many of the highest production regions worldwide (Munné-Bosch and Vincent, 2019; Reig et al., 2017). As temperatures in the majority of apple production regions are expected to continue to rise (Austin and Hall, 2001), determining and adapting integrative approaches to manage and reduce the adverse impacts of solar irradiation, both in the orchard (Morales-Quintana et al., 2020) and during the cold chain, is imperative.

Heat in combination with radiation from ultraviolet and visible regions of the spectrum are the principal causes of sunburn injuries in the orchard (Racsko and Schrader, 2012). Direct sun exposure can lead to surface temperatures that are above 52 °C resulting in baking or “sunburn necrosis” while lesser temperatures or exposure duration can result in less catastrophic injuries such as “sunburn browning” or “photooxidative sunburn”, although ultraviolet and photosynthetically active light are still required (Woolf and Ferguson, 2000; Racsko and Schrader, 2012). Many of the first reported studies of sunburn focused on reduced sensitivity to sun stress conferred by acclimation. Sudden exposure of the fruit surface to even moderate sunlight can result in sunburn disorders and, likewise, prior non-damaging exposure to less intense sunlight can reduce sunburn (Brooks and Fisher, 1926), indicating that fruit can develop a tolerance through acclimation conceivably using a variety of proposed mechanisms (Racsko and Schrader, 2012).

Sun exposure can continue to alter fruit physiology and appearance during the cold chain (Woolf and Ferguson, 2000). Sunscald, a postharvest apple peel disorder characterized by superficial darkening, typically appears after 1 month in the cold chain (Lurie et al., 1991). Sunscald symptoms express entirely on the sun-facing side of the fruit and can be eliminated by bagging fruit or reducing direct sunlight exposure (Contreras et al., 2008) demonstrating sun exposure is a principal cause. However, it is unknown which wavelengths have the most impact. Although superficial scald and delayed sunscald can appear similar, the disorders are distinctly different both etiologically and developmentally, as superficial scald develops on less sun exposed peel (Albrigo and Childers, 1970) and sunscald development is not influenced by antioxidant treatment (Lurie et al., 1991).

Sun exposure also has less obvious, yet no less profound, influences on apple quality in the cold chain. Temperature impacts maturity and overall quality even on and within the same fruit (Woolf and Ferguson, 2000). This can result in very different ripening characteristics during the cold chain and inconsistent storage outcomes among fruit receiving different amounts of sunlight. Flesh on the sun-facing side is generally more mature at harvest with more advanced starch hydrolysis, higher soluble solids, and lower titratable acidity, although flesh is typically firmer (Klein et al., 2001). Previous reports demonstrate the relationships among maturity, fruit quality, and tree position of apples (Farhoomand et al., 1977). Examination of the metabolome indicates that these differences may, at least in part, be influenced by relative sun exposure within the canopy (Serra et al., 2018).

Metabolic evaluation has been a focus of many earlier studies determining the impact of sunlight on sunburn and sunscald development and damage mediation. In apple peel, elevated H₂O₂ and malonyl dialdehyde levels (Chen et al., 2008) as well as photoinhibition (Li and Chen, 2008; Naschitz et al., 2015) are associated with sunburn, indicating an elevated reactive oxygen species load that requires quenching. Likewise, pathways involved in sun stress mediation include antioxidant systems such as ascorbate-glutathione (Ma and Cheng, 2003), ascorbate peroxidase (Zhang et al., 2014), superoxide dismutase (Andrews and Johnson, 1996), catalase (Hao and Huang, 2004), and photooxidative quenching involving the xanthophyll cycle (Ma and Cheng, 2003). A variety of other metabolites and associated processes are implicated in apple peel light response, including cuticular wax thickness and consistency (Markley and Sando, 1931; Solovchenko and Merzlyak, 2003; Shepherd and Griffiths, 2006), phytohormones (Torres et al., 2017), compatible solute production (Torres et al., 2013), and photoprotection resulting from carotenoid (Felicetti and Schrader, 2009a; Merzlyak and Chivkunova, 2000) and flavonoid (Felicetti and Schrader, 2009b; Merzlyak and Chivkunova, 2000) accumulation. Most recently, focused metabolic evaluation has revealed, similar to sunburn, links between sunscald and elevated flavonol glycoside and carotenoid levels along with reduced chlorophyll content (Hernandéz et al., 2014).

Our previous work, using less biased (untargeted or non-targeted) metabolic analyses, reflected the breadth of coordinated metabolic changes as impacted by orchard and cold chain management, including orchard light management of ‘d’Anjou’ pear (Serra et al., 2018). Using a similar strategy to many prior studies that contrast sun-facing and shaded sides of apple (Brooks and Fisher, 1926; Ma and Cheng, 2003; Li and Cheng, 2008), our objective was to determine any sequential changes during 6 months (180 days) cold air storage within pathways with reported links to sun exposure and establish new associations among metabolites impacted by relative sunlight exposure. We expected that metabolism would be altered in many pathways in a similar fashion in all 4 cultivars reflecting the enduring influence prior sun exposure has on metabolism during cold storage.