A convergence of sunlight and cold chain: The influence of sun exposure on postharvest apple peel metabolism
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.
Section snippets
Fruit sources, harvest, and sorting
Apples from four cultivars were harvested at commercial maturity from commercial orchards near Mattawa, WA, USA (‘September Wonder Fuji’, ‘Gala’, ‘Granny Smith’) and Chelan, WA, USA (‘Honeycrisp’). ‘September Wonder Fuji’ is an early maturing cultivar harvested 1–2 months before more typical ‘Fuji’ cultivars (or “strains”). Orchards with small trees were selected to obtain fruit with relatively high sun exposure. Upon harvesting only from the tree periphery, each fruit was marked on the top of
Results
Although we tracked visual phenotype, our intent was only to account for disorders, where present, while linking metabolism with relative sun exposure for all 4 cultivars. Incidence of sunburn represented in selected populations from each cultivar was different as sunburned fruit were only selected for comparison of relative sun exposure where sunburn was too prevalent to avoid in that population. Consequently, incidence of sunburn, defined as orange or brown peel discoloration at-harvest, was
Discussion
Results indicate sun exposure impacts both appearance and metabolism. While postharvest disorder development was limited to ‘Granny Smith’ sunscald and, much less prominently, expansion of lenticel blotch on ‘Honeycrisp’ peel, metabolism was strikingly different in all cultivars depending upon sun exposure. In some cases, metabolism could be easily linked with appearance in the case of chromophoric metabolites such as anthocyanin or ß-carotene. However, the majority of differential change
Funding
This work was supported by the Washington Tree Fruit Research Commission (project number: AP-16-102– “Risk assessment for delayed sunburn and sunscald”) and USDA-ARS (project number: 2094-43000-006-00D– “Developmental genomics and metabolomics influencing temperate tree fruit quality”).
CRediT authorship contribution statement
Christine K. McTavish: Investigation, Writing - original draft. Brenton C. Poirier: Investigation, Writing - review & editing. Carolina A. Torres: Conceptualization, Writing - review & editing, Funding acquisition. James P. Mattheis: Conceptualization, Writing - review & editing, Funding acquisition. David R. Rudell: Conceptualization, Investigation, Visualization, Writing - original draft, Supervision, Funding acquisition, Project administration.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We thank Edward Valdez, Garrett Britt, and Nathanael Sullivan for their expert assistance and Brent Milne of McDougal and Sons for their assistance in obtaining apples for this study.
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