Watermelon [Citrullus lanatus (Thumb.) Matsum & Nakai] is an important crop grown worldwide. The United States is the sixth largest producer in the world, with an industry value of more than $430 million and an annual production of ≈2 million metric tons (FAO, 2012; NASS, 2014). Watermelons are grown throughout the United States, with production mainly in the southern states (Wehner, 2008). Recently, watermelon has gained national attention as a good source of antioxidants (lycopene), arginine, and the arginine precursor, citrulline (Hong et al., 2015; Kaore and Kaore, 2014; Wang et al., 2014).
Lycopene is a red-pigmented carotenoid with powerful antioxidant properties that serves as an intermediate for the biosynthesis of other carotenoids (DiMascio et al., 1989; Sandmann, 1994; Tomes et al., 1963). In red-fleshed watermelon, lycopene accounts for 70% to 90% of the total carotenoids; the remaining carotenoids include phytofluene, phytoene, β-carotene, lutein, nerosporene, and ζ-carotene (Gross, 1987; Tomes et al., 1963). In orange-fleshed watermelon, prolycopene, phytoene, and ζ-carotene are the major carotenoids, whereas in canary yellow and salmon yellow-fleshed watermelons, neoxanthin is the major carotenoid (Bang et al., 2010; Tadmor et al., 2004). Studies have shown that the content of lycopene and carotenoids increases rapidly and accumulates 10–12 d after pollination in diploid watermelons and continues to accumulate as the fruit mature (Lv et al., 2015). Lycopene concentration varied widely in the watermelon cultigens tested, ranging from 36 to 120 mg·kg−1 of fresh weight and can vary among production environments (Leskovar et al., 2004; Perkins-Veazie et al., 2001, 2006). The lycopene content has generally not been measured in most commercial cultivars.
In humans, lycopene scavenges singlet oxygen and peroxy radicals, and deactivates excited molecules or DNA chain breaking agents (Stahl et al., 1997). Several epidemiology studies found that lycopene reduced cancer cell growth and induced cell death in malignant leukemia, endometrial, mammary, lung, and prostate cancer cells (Amir et al., 1999; Collins et al., 2006; Kotake-Nara et al., 2001; Muller et al., 2002). Arab and Steck (2000) and Matos et al., (2000) reported that lycopene attached to low-density lipoproteins in blood plasma and protected against lipid peroxidation and foam cell production, both of which are implicated in the initiation of atherosclerosis. In other epidemiological studies, Steinmetz and Potter (1996) and Strandhagen et al. (2000) found that a diet consisting of fruits and vegetables rich in lycopene could protect against stroke and cardiovascular diseases, whereas Tarazona-Diaz et al. (2013) determined that watermelon juice containing lycopene and citrulline could improve athlete recovery and performance.
Besides lycopene, watermelons produce L-arginine (arginine) and its precursor L-citrulline (citrulline) in fruit and foliage (Akashi et al., 2001; Davis et al., 2011). In related Citrullus species, studies have shown that citrulline content increases in the foliage during drought stress and may improve plant tolerance to stress (Akashi et al., 2001; Wang et al., 2014). Similarly in melon, foliage citrulline content is an important indicator for drought stress (Kusvuran et al., 2013). In developing watermelon fruit, citrulline content is low, reaching peak levels just before maturity, and declining as fruit ages (Fish, 2014). In fruit, the value of citrulline accumulation as a stress tolerance is unknown.
In mammals, arginine plays an essential role in the nitric oxide pathway, contributing to improved immune processes and cardiovascular health. In rats, consumption of watermelon extracts with high citrulline resulted in improved lipid profiles, lower inflammation, and higher antioxidant capacity (Hong et al., 2015). In mice, hypothermia recovery and vascular endothelium function were improved in subjects administered a 1% dose of citrulline (Kobayashi et al., 2014). Free arginine, administered through supplements, can result in side effects such as nausea and gastrointestinal discomfort, prompting physicians to seek alternative forms of arginine (Collins et al., 2007; Hong et al., 2015). In humans, the arginine precursor, citrulline, is converted into arginine via argininosuccinate synthase (Collins et al., 2007).
In watermelon, citrulline has not been associated with fruit phenotypic traits such as flesh color (red, orange, salmon yellow, or white) (Davis et al., 2011). Previously, citrulline content was evaluated in 56 watermelon cultigens (cultivars, breeding lines, and PI accessions) at two locations in Texas and Oklahoma (Davis et al., 2011). Citrulline concentration varied greatly among cultigens. The highest citrulline concentrations were found in ‘Tom Watson’, PI 306364 (Northern Africa) and ‘Jubilee’, whereas the lowest citrulline concentrations were found in PI 164992 (Turkey), Low Sugar 177, and Low Sugar 194. These data suggest that citrulline has likely not been indirectly selected by breeders during cultivar development. Both unadapted lines and commercial cultigens may have useful variation in citrulline content. The variation in arginine content has not been directly evaluated in watermelon to date.
Watermelon breeding has resulted in a diversity of fruit sizes, rind color, rind patterns, and flesh color. Most cultivars have soluble solids content (°Brix) between 8% and 15% and acidity (flesh pH) of 5.18–5.60 (Corey and Schlimme, 1988). Studies have shown that variation in citrulline and lycopene exist within cultivated watermelons, but wild relatives and heirloom cultivars can also serve as good sources of trait variation for genetic improvement (Wehner, 2008). Many of these wild and weedy relatives have undesirable characteristics such as high or low flesh pH or low sugar content. Estimates of heritability and correlations among traits can help in the selection of breeding strategies and selection of parent material. Few studies to date have looked at the heritability and correlation of health compounds such as lycopene, arginine, and citrulline with fruit quality traits such as percent soluble solids and flesh acidity. The objectives of this study were to a) evaluate a diverse set of watermelon cultigens for lycopene, citrulline, and arginine content; b) determine the heritability of those traits; and c) measure the correlation of health compound concentrations with fruit acidity and soluble solids content.
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