Chemical and Sensory Properties of Greenhouse Tomatoes Remain Unchanged in Response to Red, Blue, and Far Red Supplemental Light from Light-emitting Diodes

In addition to photosynthesis, light is a critical mediator of secondary metabolism in plants, signaling the production of potentially health-promoting phytochemicals and regulating the emission of volatile organic compounds (VOCs) that can alter the sensory perception of a tomato. Light-emitting diodes (LEDs) are a viable way to test the effects of individual wavebands of light and are being quickly adopted by the greenhouse tomato industry. However, studies characterizing the effects of specific wavelengths of light or supplemental lighting on phytochemical content in general are lacking. We hypothesized that enriching the amount of supplemental blue and/or red light that tomatoes receive would positively affect the amount of carotenoids and phenolic compounds that accumulate in tomato fruits through cryptochrome and/or phytochrome-dependent signaling pathways. To test this hypothesis, we compared the chemical and sensory characteristics of tomatoes grown with overhead high-pressure sodium (OH-HPS) lamps to those grown with intracanopy (IC)-LEDs emitting different ratios of red, blue, and far red light. Tomatoes were profiled for total soluble solids, titratable acidity, ascorbic acid content, pH, total phenolics, and prominent flavonoids and carotenoids. Our studies indicated that greenhouse tomato fruit quality was only marginally affected by supplemental light treatments. Moreover, consumer sensory panel data indicated that tomatoes grown under different lighting treatments were comparable across the lighting treatments tested. Our research suggests that the dynamic light environment inherent to greenhouse production systems may nullify the effects of wavelengths of light used in our studies on specific aspects of fruit secondary metabolism. Plants are sessile organisms that use numerous mechanisms to respond to dynamic environmental factors. One such factor is light, which is a powerful elicitor of primary and secondary metabolism that ultimately affects the chemical and sensory properties of edible plant tissues. Alterations in metabolic flux in response to light are mediated by a host of proteins including the phytochromes, cryptochromes, phototropins, and UVR8, among others (Galv~ao and Fankhauser, 2015; Gyula et al., 2003; Rizzini et al., 2011). To test hypotheses about effects of specific wavelengths on plant primary and secondary metabolism, photobiologists have leveraged LEDs for more than 20 years to tease apart complex, light-driven processes (Barta et al., 1992; Bula et al., 1991). Moreover, this technology is being adopted by the greenhouse tomato industry as an efficient alternative to high-pressure sodium fixtures commonly used to provide supplemental light during low-light periods of the year. LEDs are gaining popularity not only because of their gradually increasing energy efficiency but also because of their long life span, relatively cool emitting surfaces, and ability to emit narrow-waveband light (Morrow, 2008; Nelson and Bugbee, 2014). Different qualities and quantities of light can influence not only growth and development but also secondary metabolic processes that determine nutritive value and flavor attributes. This research spans many high-value crops including arugula (Eruca sativa) (Mattson and Harwood, 2012), broccoli microgreens (Brassica oleracea) (Kopsell and Sams, 2013), cabbage (Mizuno et al., 2011), lettuce (Lactuca sativa) (Li and Kubota, 2009; Stutte et al., 2009), kale (Carvalho and Folta, 2014b; Lefsrud et al., 2008), and tomato (Gautier et al., 2005b) among many others. Further examples of light influencing produce quality have been well reviewed (Carvalho and Folta, 2014a; Mitchell et al., 2015). The effects seen in these studies are frequently related to changes in ascorbic acid, carotenoids, and polyphenolic compounds. Ascorbic acid (vitamin C) is a cofactor for many metabolic processes, serves as an antioxidant, and is an essential nutrient for humans (Laing et al., 2007). Ascorbic acid accumulation in tomatoes has been shown to be a function of fruit irradiance, creating the possibility to use intracanopy lighting (ICL) with LEDs to increase concentrations in tomato fruits (Gautier et al., 2009). Tomatoes also contain bioactive flavonoids such as quercetin-3-O-rutinoside (rutin) and kaempferol-3-O-rutinoside that have been associated with several positive health benefits (Gonz alez et al., 2011; Kauss et al., 2008; Naderi et al., 2003; Raiola et al., 2014; Spencer, 2009). The biosynthesis of these compounds can also be modulated in response to light (Jagadeesh et al., 2009; Li and Kubota, 2009; Ordidge et al., 2010; Stutte et al., 2009). Last, tomatoes are an excellent source of carotenoids, most notably lycopene, which are associated with reduced risk for cardiovascular disease and some cancers (Ciccone et al., 2013; Gonz alezVallinas et al., 2013). Blue, red, and far red light have been shown to alter tomato fruit concentrations of both lycopene and b-carotene (Alba et al., 2000; Gautier et al., 2011, 2008). Manipulating flavonoids and carotenoids in tomato fruits could also indirectly alter the concentrations of VOCs that are produced from these same pathways (Baldwin et al., 1991; Tieman et al., 2006). However, limited studies exist relating light quality to tomato fruit composition and sensory properties. We hypothesized that direct irradiation of tomato fruit clusters with supplemental light would alter the concentrations of ascorbic acid, carotenoids, and polyphenolic compounds depending on the quality of light used. To test these hypotheses, we supplemented greenhouse tomatoes grown using commercial practices with different qualities of light from HPS fixtures or custom-built IC-LED towers. One variety was also grown Received for publication 6 Sept. 2017. Accepted for publication 9 Nov. 2017. Funding was from the USDA NIFA-SCRI program (2010-51181-21369). We thank Judy Santini for statistical consulting, as well as Sydney Moser and Ben Redan for guidance in the quantification of flavonols. We also thank Rob Eddy, DanHahn, EricWhitehead, DanMartin, Roger Rozzi, and Joe Littiken for their help in greenhouse studies. Corresponding author. E-mail: michaelpdz@ gmail.com. 1734 HORTSCIENCE VOL. 52(12) DECEMBER 2017 outdoors to establish a ‘‘garden-grown’’ quality benchmark in Expt. 1. Tomatoes were then tested using several physicochemical quality metrics including total soluble solids, citric/ascorbic acid content, pH, total phenolics, and prominent flavonoids and carotenoids. We also included a consumer sensory panel in Expt. 2 to gauge how ratios of red, blue, and far red light affect the sensory attributes of greenhouse-grown tomatoes. Materials and Methods Plant materials and growing conditions. For Expt. 1, ‘Komeett’ tomato seeds (De Ruiter Seeds, Columbus, OH) were sown into Agrifoam soilless plug strips (SteadyGROWpro; Syndicate Sales, Kokomo, IN) in late Spring 2014 in a glass-glazed greenhouse located in West Lafayette, IN (lat. 40 N, long. 86 W; USDA hardiness zone 5b). Fertigation was carried out on an as-needed basis using an acidified fertilizer solution that contained a 3:1 mixture of 15N–2.2P–12.5K and 21N–2.2P–16.6K, respectively, providing 200 N-NO3, 26 P, 163 K, 50 Ca, 20 Mg, and micronutrients (mg·L; The Scotts Co., Marysville, OH). Plants were transferred into rooting blocks (SteadyGROWpro; Syndicate Sales) and placed onto wetted coconut coir slabs (Riococo 200; Ceyhinz Link International, Inc., Dallas/Fort Worth, TX). Slabs were placed onto steel gutters (9.8 m · 25 cm; FormFlex Horticultural Systems, Ontario, Canada), aligned east–west, and plant density was 2.2 stems/m. Plants were irrigated using a commercially standard fertilizer mix (4.5N–14P–34K; CropKing, Lodi, OH) and irrigation frequency was adjusted as needed to maintain a daily leaching fraction (LF) of 30% (4.5N–14P–34K; CropKing). Electrical conductivity (EC) and pH of the influx and efflux were tested each day using a hand-held EC and pH meter (Hanna Instruments, Woonsocket, RI) and fertigation adjusted as needed to ensure that values were maintained within recommended ranges (2.5–3.5 dS·m and 5.8–6.3 for EC and pH, respectively) (Jones, 2008). Average day/night greenhouse temperatures were set to 25/15 C, respectively. Plants were trellised on a high-wire system, and the experiment was conducted between July and Nov. 2014. To establish a ‘‘garden-grown’’ control, ‘Komeett’ plants were also grown in an outdoor field site. Seedlings were cultured similarly as described previously but transferred to a field site with cambric-loam soil previously amended with organic compost after 5weeks of growth in late Spring 2014. Plants were staked using the ‘Florida Weave’ method and weeds were suppressed using heavy-duty weed cloth (FarmTek, Dyersville, IA). For Expt. 2, ‘Merlice’ (De Ruiter Seeds) tomato plants were cultured similarly to plants in Expt. 1 except that they were started in early Dec. 2014, grafted onto ‘Maxifort’ (De Ruiter Seeds) rootstocks, pruned to have two leading heads per plant, the steel gutters were arranged facing north–south, and the experiment lasted 5 months. Lighting treatments. For Expt. 1, the greenhouse was divided into three blocks using movable double-layered 6-mil (150 mm) white polyethylene plastic curtains that were 3.6 m in height (Supplemental Table 1; Supplemental Figs. 1 and 2). When supplemental lighting was inactive, the curtains were withdrawn to allow for maximum transmission of solar photosynthetically active radiation (PAR) into crop canopies. Each block was divided into four 1.8 · 2.4-m sections allowing for four different treatments to be represented in each block. Each section was divided by a piece of white polyethylene large enough to reduce light pollution between treatments within a block but not to inhibit airflow within the greenhouse. Eight double-headed plants were grown within each supplemental lighting treatment. In Expt. 1, s