Fruit of jujube cultivars Li, Lang, Sugarcane, and September Late sampled from Alcalde, NM, at different harvest dates in 2018 and 2019. ND = no data.
Fruit of different jujube cultivars at different maturity sampled from Las Cruces (LC), Los Lunas (LL), and Alcalde (AL), NM, in 2019.
(A) Total phenolic content (TPC), (B) proanthocyanidins (PA), (C) antioxidant activity, (D) ferric reducing antioxidant potential (FRAP), (E) moisture, and (F) vitamin C in fruit of different jujube cultivars at creamy and full-red maturity harvested from Alcalde, NM, in 2018 and 2019. Different letters denote a significant difference at P < 0.05. AAE = ascorbic acid equivalent; DPPH = 2,2-diphenylpicrylhydrazyl; DW = dry weight.
Dynamics of cyclic adenosine monophosphate with maturity in different jujube cultivars harvested from Alcalde, NM, in 2018. Different lowercase letters for each cultivar denote a significant difference across harvest dates at P < 0.05. DW = dry weight.
Dynamics of cyclic adenosine monophosphate with maturity in different jujube cultivars harvested from Las Cruces, NM, in 2019. Different lowercase letters for each cultivar denote a significant difference across harvest dates at P < 0.05. Different uppercase letters at each harvest date indicate a significant difference among cultivars at P < 0.05
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Jujube (Ziziphus jujuba Mill.) is also called Chinese date. There are ∼100 jujube cultivars with limited commercial availability, and the majority of them have scant details in the United States. In this study, nutrient dynamics during fruit maturation of different jujube cultivars grown at Las Cruces, Los Lunas, and Alcalde, NM, were examined in 2018 and 2019. Cultivars varied by location and year, and included ‘Li’, ‘Lang’, ‘Sugarcane’, ‘September Late’, and ‘Sherwood’. Parameters tested were total phenolic content (TPC), proanthocyanidins (PAs), vitamin C, cyclic adenosine monophosphate (cAMP), and antioxidant capacity: 2,2-diphenylpicrylhydrazyl radical scavenging capacity and ferric reducing antioxidant potential (FRAP). Moisture, TPC, PAs, FRAP, and vitamin C content decreased with fruit maturity; however, the latter stage of fruit maturity showed an increase in cAMP. Compared with fruit at full-red maturity, creamy fruit had TPC, PA, FRAP, and vitamin C concentrations that were 1.0 to 1.8, 4.4 to 12.4, 1.9 to 2.6, and 0.1 to 1.3 times higher, respectively, depending on location (P < 0.05). From creamy to full-red maturity, cAMP increased by 0.9 to 4.5 times. At full-red maturity, estimated TPC in jujube fruit ranged from 10.6 to 16.8 mg gallic acid equivalent per gram dry weight (DW), whereas estimated PAs ranged from 1.8 to 5.3 mg PA B2/g DW. Jujube fruit at full-red maturity had a vitamin C content that ranged from 649.0 to 1153.3 mg/100 g DW. At full-red maturity, the concentration of cAMP ranged from 148.1 to 277.6 μg/g DW in Las Cruces samples.
Ziziphus jujuba Mill., commonly known as Chinese date, or red date, originated in China more than 4000 years ago, where more than 800 cultivars are reported (Chen et al. 2013). It is a nutritionally important fruit crop that belongs to the Rhamnaceae family. Jujube has been proposed as a superfruit—a fruit that meets the diverse needs of growers, consumers, marketers, governments, and society, now and in the future (Liu et al. 2020). Dry jujube fruit are widely used in traditional Chinese medicine (Guo and Shan 2010; Li et al. 2007). Jujube is a multipurpose fruit crop with diverse uses (Sheng and Shen 2011). Commercially, jujube fruit are marketed as fresh and dry fruit, consumed as snacks. However, jujube can also be used as a food additive or flavoring in processed, value-added products (Gao et al. 2013; Guo and Shan 2010).
Potential health benefits of jujube have been attributed to bioactive compounds such as phenolics, vitamin C, and cyclic adenosine monophosphate (cAMP). Jujube is a very good source of vitamin C and cAMP, which exhibit various health benefits (Guo et al. 2015; Huang et al. 2017; Zhao et al. 2009). Jujube also contains other beneficial compounds such as triterpenic acids, fiber (soluble and insoluble), volatile compounds, and minerals (potassium, phosphorus, calcium, and manganese) (Guo et al. 2015; Li et al. 2007).
In the United States, commercial jujube cultivars were first introduced in 1908 by US Department of Agriculture agricultural explorer Frank N. Meyer, who predicted its suitability for the semiarid South and Southwest (Yao 2013). There are currently ∼100 jujube cultivars in the United States, but none has been released with comprehensive information. In general, jujube research has been limited in the United States (Kader 1982; Locke 1948; Lyrene 1983). In 2011, the New Mexico State University (NMSU) Sustainable Agriculture Science Center at Alcalde imported more than 30 cultivars directly from China and carried out research on them (Yao 2013). Replicated jujube cultivar trials were set up at NMSU’s Alcalde (2015), Los Lunas (2015), and Leyendecker (in Las Cruces) (2017) centers (Yao et al. 2020). Cultivar, fruit maturity, and location have all been reported to affect the nutrient profile and content in jujube fruit (Gao et al. 2013; Guo et al. 2015; Huang et al. 2017; Kou et al. 2015). There are very few studies with jujube cultivars propagated and tested in the United States, even though many have been done with various jujube cultivars from around the world (Huang et al. 2017). In light of this, we decided to evaluate the dynamics of various compounds, including moisture, total soluble solids (TSS), total phenolic content (TPC), proanthocyanidins (PAs), antioxidant activity, and cAMP, in different American jujube cultivars from different locations: Las Cruces, Los Lunas, and Alcalde, NM.
In 2018, jujube fruit were sampled from NMSU’s Sustainable Agriculture Science Center at Alcalde, NM (lat. 36°05′27.94″N, long. 106°03′24.56″W; elevation, 1730 m). Three trees of four cultivars—Li, Lang, September Late, and Sugarcane—were selected randomly from the same orchard planted in 2011 and sampled at 14-d intervals from 28 Aug to 9 Oct as applicable. Fruit of ‘Lang’ and ‘Sugarcane’ were sampled from 28 Aug to 25 Sep, whereas ‘Li’ and ‘September Late’ were sampled from 28 Aug to 9 Oct. The varying maturation dates of different jujube cultivars accounted for the variation in sampling finish date.
In 2019, three different trees of each jujube cultivar from three different locations—Las Cruces, Los Lunas, and Alcalde—were sampled from August to October. Jujube grown at the NMSU Leyendecker Plant Science Research Center at Las Cruces, NM (lat. 32°12′08.9″N, long. 106°44′41.4″W; elevation, 1176 m), and the NMSU Agricultural Science Center at Los Lunas, NM (lat. 34°46′04.7″N, long.106°45′45.7″W; elevation, 1478 m), were sampled at 14-d intervals from 2 Aug to 13 Sep and 2 Aug to 27 Sep, respectively. Grafted trees at Los Lunas were planted in 2012, and in 2017 at the Leyendecker location. Jujube fruit from the Sustainable Agriculture Science Center at Alcalde, NM, were sampled at 14-d intervals from 16 Aug to 11 Oct. In 2019, ‘Li’, ‘Lang’, and ‘Sherwood’ fruit were sampled from Las Cruces; Li, Lang, and Sugarcane fruit were sampled from Los Lunas; and ‘Li’, ‘Lang’, ‘Sugarcane’, and ‘September Late’ fruit were sampled from Alcalde. Fruit from 2-year-old or older branches were sampled to avoid any possible discrepancy in nutrient content resulting from branch age. Fruit sampled on the same harvest date were at different maturity stages depending on the cultivar (Fig. 1), and different maturities occurred within cultivars at different sampling dates depending on the location (Fig. 2). Harvested samples free from diseases and blemishes were used for analysis.
Citation: HortScience 58, 2; 10.21273/HORTSCI16880-22
Citation: HortScience 58, 2; 10.21273/HORTSCI16880-22
Fruit samples were transported on ice to the laboratory at NMSU in Las Cruces. Pictures of jujube fruit from each cultivar at each harvest date were taken using a digital single-lens reflex camera under ambient lighting in the laboratory. In the laboratory, jujubes were deseeded, freeze-dried (HarvestRight, North Salt Lake, UT, USA) for 48 h at –55 °C until they reached a final moisture content of less than 5%, and ground to a fine powder using a coffee grinder (Hamilton Beach, Glen Allen, VA, USA). Jujube powder from 2018 samples were stored at –18 °C, whereas 2019 jujube powdered samples were stored at –57 °C until further analysis.
Gallic acid, Folin–Ciocalteu reagent, PA B2, sodium carbonate, 2,2-diphenyl-1-picryl-hydrazyl (DPPH), ferric reducing antioxidant potential (FRAP) reagent, ascorbic acid standard, 2,6 dichlorophenolindophenol, and adenosine 3′,5′-cyclic monophosphate was purchased from Sigma Aldrich (Burlington, MA, USA). All other chemicals were also analytical grade and were obtained from Sigma Aldrich.
Moisture content of jujube fruit was measured using the oven drying method. The weight difference of the sample was recorded after drying in a convective oven (Baker’s Pride, Smithville, TN, USA) at 65 °C until the weight remained constant. Measurements were recorded as the percentage of moisture of the fresh weight (FW).
The percentage of TSS content was measured using a digital refractometer (PAL-3; Atago Instruments, Bellevue, WA, USA) as described by Huang et al. (2017).
Fifteen to 20 fruit sampled from each cultivar (n = 3) were weighed, and weight per fruit was measured in grams.
For extract preparation, 1.5 g freeze-dried jujube powder was homogenized in 15 mL of 80% ethanol for 1 min using a polytron homogenizer (Kinematica CH-6010; Bohemia, NY, USA), followed by sonication in an ultrasonic water bath (Ultrasonic bath 15337426; Fischer Scientific, Pittsburgh, PA, USA) at room temperature for 30 min. Supernatant filtered through 0.45 µm polyvinylidene fluoride (PVDF) syringe filters was used for the analysis of TPC, PAs, and antioxidant capacity.
TPC content of jujube fruit was determined using the Folin–Ciocalteu spectrophotometric method described by Wang et al. (2011), with a few modifications. Folin–Ciocalteu reagent (0.5 mL) was added to 0.5 mL of appropriately diluted sample and mixed thoroughly. The mixture was kept in the dark at room temperature for 5 min. Then, 1.5 mL of sodium carbonate (20%) was added to the mixture and vortexed. Next, the total volume of mixture was adjusted to 10 mL with deionized water and mixed. The mixture was incubated at 75 °C for 10 min, and the absorbance reading was recorded using a spectrophotometer (ultraviolet-1800; Shimadzu, Kyoto, Japan) at a 760-nm wavelength. The gallic acid standard calibration (20, 40, 60, 80, 100, and 120 µg/mL) curve was used to quantify TPC expressed as milligrams of gallic acid equivalent (GAE) per gram of dry weight (DW).
PAs were determined using the vanillin colorimetric method described by Prior et al. (2010), with some modifications. Dimethylacetamide reagent (3 mL) was added to 1 mL of appropriately diluted sample and mixed thoroughly. The mixture was then incubated at room temperature, and the absorbance reading at 640 nm was recorded within 15 to 25 min and corrected against a blank. The PA B2 standard calibration (1.25, 2.5, 5, 10, 20, and 40 µg/mL) curve was used for quantification. PA content was expressed as the PA B2 equivalent per gram DW.
Scavenging activity of jujube extracts on DPPH was analyzed using the method reported by Wang et al. (2011), with minor modifications. Briefly, 0.1 mL of extract was mixed with 3 mL of 0.1 mM ethanolic (80%) solution of DPPH radical. The solution was kept in the dark at room temperature for 15 min, and the absorbance was read at 517 nm against an ethanol blank using a spectrophotometer. DPPH was expressed as the percentage of inhibition of DPPH. The calculation was done using where A0 is the absorbance of the control DPPH solution at 0 min and A1 is the absorbance in the presence of the test sample at 15 min.
A FRAP assay was performed according to the method described by Wang et al. (2011). FRAP reagent was prepared by mixing 2.5 mL of a 10 mM 2,4,6-Tri(2-pyridyl)-s-triazine solution in 40 mM HCl with 2.5 mL of 20 mM FeCl3 6H2O and 25 mL of 0.3 M acetate buffer; a pH of 3.6 was used for the analysis. Appropriately diluted phenolic extract (0.1 mL) was added to 4 mL of FRAP reagent preheated at 37 °C and mixed thoroughly. The mixture was incubated at 37 °C for 4 min, and the absorbance was measured at 593 nm against the blank prepared using deionized water. A standard curve was prepared using ascorbic acid at a concentration of 10.9 to 350 μg/mL. FRAP values are expressed on a DW basis as milligrams ascorbic acid equivalent (AAE) per gram of jujube sample.
The vitamin C content was determined by the visual titration method based on the reduction of 2,6-dichlorophenolindophenol dye described by Kou et al. (2015), with modifications. Briefly, 1 g of homogenized fruit sample was blended with 20 mL of 2% oxalic acid solution. Three milliliters of filtered solution was diluted to 10 mL with 2% oxalic acid and titrated with 0.717 mmol/L 2,6-dichlorophenolin-dophenol to the endpoint. The 2,6-dichlorophenolindophenol solution was calibrated with 200 μg/mL ascorbic acid. The results were expressed as milligrams per 100 g on a DW basis.
Extracts for cAMP were prepared with 15 mL of ultrapure deionized water added to 1.5 g of jujube powder. The sample–solvent mixture was homogenized for 1 min using a polytron homogenizer, followed by sonication for 30 min in an ultrasonic water bath at room temperature. The sample–solvent mixture was then centrifuged at 4500 rpm for 10 min at room temperature. Supernatants filtered through 0.2-µm PVDF syringe filters were analyzed on a Waters Acquity high-performance liquid chromatography (HPLC) system (Waters corporation, Milford, MA, USA) coupled with Quattro Ultima mass spectrometer (Wythenshawe, Manchester, UK). For each analysis, 0.01 mL of sample was used. A SynergiTM column (2 × 50 mm, 2.5 μm; Phenomenex Inc., Torrance, CA, USA) was used with 0.1% aqueous formic acid (A) and methanol with 0.1% formic acid (B) as the mobile phase for the separation of cAMP. The flow rate was 1 mL/min. Elution gradients were 80% A and 20% B (0–1 min), 100% B (1–4 min), and 80% A and 20% B (4–12 min). cAMP content in samples was quantified using a cAMP standard calibration curve of concentrations 0.78 to 100 µg/mL.
Statistical analyses were performed using SAS version 9.4 (SAS Institute, Cary, NC, USA) software. The significance level was set at P = 0.05. Different nutrient parameters were analyzed separately by location and year using a mixed model, with fixed effects for cultivar, harvest date, and their interaction, and fitting a random effect and the autoregressive covariance structure model to the repeated measures from an individual tree. Denominator degrees of freedom were computed using the Kenward–Roger method: KR 1. Despite missing cells (i.e., missing combination of cultivar and week) in Alcalde in 2018 because the interaction effect of the harvest date and cultivar for each variable measured was significant, no remedial action was required. Instead, when the interaction was significant, the least square means were calculated and least significant difference lines for the simple effects of cultivar and week were determined for each set of comparisons defined by a level of either cultivar or week. In the absence of interaction, means separation was applied to least square means corresponding to significant main effects. A secondary analysis of all variables in samples from Alcalde in 2018 and 2019 was performed based on two different edible maturity stages: creamy (with a creamy peel color) and full red for cultivars Li, Lang, and Sugarcane. Variables were analyzed using a mixed model that had fixed effects for cultivar, year, maturity stage, and all interactions, and accounted for maturity repeated measures within a year with a random effect for replication (tree) within year and cultivar. When either the three-way interaction or multiple two-way interactions were significant, Tukey adjusted means separation was conducted on the cultivar × year × maturity estimates.
Jujube fruit from Las Cruces reached full-red maturity about 2 weeks earlier than Los Lunas and 4 weeks earlier than Alcalde (Fig. 2). TSS content increased with fruit maturity (data not shown). In 2019, TSS content in ‘Li’, ‘Lang’, and ‘Sherwood’ samples at full-red maturity from Las Cruces was 26.7%, 34.1%, and 32.0%, respectively. At full-red maturity, TSS content in ‘Li’ and ‘Sugarcane’ sampled from Los Lunas were 29.2% and 25.4%, whereas ‘Li’, ‘Lang’, and ‘Sugarcane’ from Alcalde at full-red maturity had a TSS content of 22.7%, 28.2%, and 22.1%, respectively.
Regardless of location, fruit weight increased with maturity. However, there was no significant difference in average fruit weight among samples harvested on the last two to three harvest dates depending on location and cultivar (data not shown). From Las Cruces, at full-red maturity (13 Sep), ‘Li’ had a significantly greater average fruit weight compared with ‘Lang’ and ‘Sherwood’. Regardless of the harvest date/maturity, ‘Li’ had a significantly greater average fruit weight, followed by ‘Lang’ and ‘Sugarcane’ from Los Lunas. At Alcalde, at each harvest date, there was no significant difference in average fruit weight between ‘Li’ and ‘Lang’. The average fruit weight estimates of full-red ‘Lang’ and ‘Li’ from Las Cruces and Los Lunas ranged from 18.2 to 29.0 g (SE = 1.13) and 21.9 to 31.0 g (SE = 0.83), respectively, whereas Alcalde samples had fruit weight estimates ranging from 16.7 to 17.8 g (SE = 0.60).
Moisture content in jujube fruit of all cultivars—Li, Lang, Sugarcane, and September Late—from Alcalde decreased significantly across harvest dates in 2018 and 2019 (Tables 1 and 2). Although moisture content decreased steadily across sampling dates in 2018, in 2019 only samples from the creamy stage (on 13 Sep) showed a substantial decrease in moisture content (Table 2). Common cultivars Li, Lang, and Sugarcane from Alcalde at the creamy stage had moisture that varied from 82.5% to 85.1% and 83.7% to 85.0%, respectively, in 2018 and 2019, whereas at the full-red maturity stage moisture ranged from 62.7% to 69% and 66.0% to 74.2%, respectively, in 2018 and 2019 (Fig. 3E). In both years, ‘Sugarcane’ displayed a greater moisture content at full-red maturity than ‘Lang’ (Fig. 3E).
Citation: HortScience 58, 2; 10.21273/HORTSCI16880-22
Samples from Las Cruces showed a decreasing trend of moisture (Table 3). The interaction effect of cultivar × harvest date was not significant. For ‘Li’, ‘Lang’, and ‘Sugarcane’, the moisture least square means were 74.5%, 69.9%, and 73.3% (SE = 0.71), respectively, with ‘Lang’ having a significantly less moisture content relative to the other two tested cultivars. Across the harvest dates, moisture least square means were 80.8%, 76.2%, 67.6%, and 65.7% (SE = 0.78), respectively.
From the creamy stage (30 Aug), the moisture level in Los Lunas samples revealed a substantial difference across harvest dates (Table 4). Moisture content ranged from 76.5% to 81.2% and 60.5% to 68.6%, respectively, at the creamy and full-red maturity stages. When compared with other cultivars studied, ‘Li’ had a significantly greater moisture content at the creamy stage (30 Aug), whereas ‘Sugarcane’ had a greater moisture content at full-red maturity (27 Sep).
With fruit maturity, TPC in jujube fruit decreased. At the creamy and full-red maturity stages, TPC in Alcalde jujube in 2018 ranged from 26.4 to 33.4 mg GAE/g DW and 13.4 to 16.4 mg GAE/g DW, respectively (Table 1). Across harvest dates in 2019, TPC in Alcalde samples showed a declining trend. TPC was between 29.8 and 34.5 mg GAE/g DW at creamy maturity (13 Sep), and 15.2 and 16.8 mg GAE/g DW at full-red maturity (11 Oct) (Table 2).
At the creamy stage, ‘Li’ had the greatest TPC compared with other cultivars, whereas at full-red maturity, there was no significant difference among ‘Li’, ‘Lang’, and ‘Sugarcane’. There was no significant difference in TPC between Alcalde samples from 2018 and 2019 when the cultivars were examined at full-red maturity (Fig. 3A).
At Las Cruces, TPC showed a decreasing trend across harvest dates in 2019 (Table 3). The interaction effect of cultivar and harvest date was not significant for Las Cruces samples (P = 0.058). There was no significant difference in TPC among cultivars, with TPC least square means for ‘Li’, ‘Lang’, and ‘Sugarcane’ being 19.2, 18.2, and 18.5 mg GAE/g DW (SE = 0.82), respectively.
TPC from Los Lunas in 2019 also showed a decreasing trend (Table 4) as maturity progressed. At the creamy stage (30 Aug), ‘Li’ had a significantly greater TPC than ‘Lang’ and ‘Sugarcane’, and at full-red maturity (27 Sep) there was no significant difference in TPC among cultivars (Table 4).
In 2019, TPC in jujube at the creamy stage sampled from Las Cruces, Los Lunas, and Alcalde ranged from 25.8 to 30.2, 22.7 to 29.9, and 20.2 to 34.5 mg GAE/g DW, respectively, whereas at full-red maturity, TPC ranged from 10.6 to 11.4, 10.9 to 12.9, and 15.2 to 16.8 mg GAE/g DW, respectively.
Except for ‘September Late’ for the first two harvest dates (28 Aug and 11 Sep), all jujube cultivars sampled from Alcalde in 2018 showed a significant decrease in PAs across harvest dates (Table 1). In 2019, PAs decreased after the creamy stage (13 Sep) for all cultivars (Table 2). At the creamy stage, PA estimates ranged from 17.2 to 34.2 mg PA B2/g DW, whereas at full-red maturity (11 Oct) PA estimates ranged from 1.8 to 5.3 mg PA B2/g DW. Among ‘Li’, ‘Lang’, and ‘Sugarcane’, PAs did not differ significantly at full-red maturity (11 Oct) and when all cultivars were at the creamy stage (13 Sep) (Table 2). At the creamy stage, PAs for each cultivar were significantly greater in samples from Alcalde in 2019, whereas at full-red maturity there was no significant difference in PAs among cultivars or between 2018 and 2019 (Fig. 3B).
Fruit sampled from Las Cruces in 2019 showed a decreasing trend of PAs across harvest dates (Table 3). At the first harvest date (2 Aug) when fruit for all cultivars were at the creamy stage, ‘Lang’ had significantly greater PAs compared with ‘Li’ and ‘Sherwood’, but cultivar differences were not detected at full-red maturity on 13 Sep. Depending on the cultivar, the PA estimated content in creamy fruit ranged from 26.4 to 34.3 mg PA B2/g DW. The PA estimates ranged from 4.0 to 4.9 mg PA B2/g DW at full-red maturity.
There was a steep decrease in PAs in samples from Los Lunas across harvest dates (Table 4). Interaction effect of cultivar × harvest date was not significant (P = 0.19), and least square means across harvest dates were 42.6, 33.5, 22.2, 7.7, and 2.8 mg PA B2/g DW (SE = 1.09). Least square means for ‘Li’, ‘Lang’, and ‘Sugarcane’ were 26.8, 20.4, and 18.0 mg PA B2/g DW (SE = 0.90), respectively, whereas ‘Li’ demonstrated significantly greater PAs among cultivars. PA levels ranged from 17.7 to 27.7 and 2.1 to 3.9 mg PA B2/g DW in fruit at the creamy and full-red maturity stages, respectively.
In 2018, only ‘Sugarcane’ showed a significant decrease in DPPH across all harvest dates (Table 1). For ‘Li’, ‘Lang’, and ‘September Late’, samples on the second harvest date (11 Sep) had the greatest DPPH value; for ‘Sugarcane’, fruit sampled on 28 Aug had the greatest DPPH value. In 2019, Alcalde samples did not have a cultivar × harvest date interaction effect (P = 0.26) (Table 2). Overall, DPPH estimates were significantly greater for ‘Li’ and significantly less for ‘September Late’, with values of 88.7% and 83.8% (SE = 0.46), whereas ‘Lang’ and ‘Sugarcane’ had similar estimates at 85.7% and 85.3%, respectively. The sampling date main effect was also significant, with later dates 13 Sep, 27 Sep, and 11 Oct having greater estimates (86.4–87.6%) than earlier dates (84.3–84.4%). For Alcalde, at the creamy stage ‘Li’ had greater DPPH in 2018 than 2019 (Fig. 3C). At full-red maturity, ‘Li’ and ‘Sugarcane’ had greater DPPH in 2018, whereas there was no significant difference in DPPH between 2018 and 2019 samples for ‘Lang’ (Fig. 3C).
In 2019, ‘Sherwood’ from Las Cruces did not show a significant difference in DPPH across all harvest dates, whereas ‘Lang’ showed no significant difference in DPPH on three harvest dates (Table 3). Only ‘Li’ had a significant difference in DPPH across harvest dates from the second harvest date (16 Aug). At both creamy and full-red maturity, ‘Lang’ had the greatest DPPH value numerically compared with other cultivars (Table 3).
In 2019, there were no significant differences in DPPH across the last three harvest dates within cultivars at Los Lunas (30 Aug, 13 Sep, and 27 Sep) (Table 4). At creamy and full-red maturity, ‘Li’ had the greatest DPPH value numerically compared with other cultivars (Table 4).
In 2018, fruit harvested from Alcalde had a decreasing trend in FRAP with maturity for all cultivars (Table 1). FRAP values at the creamy stage ranged from 52.3 to 70.5 mg AAE/g DW, with ‘Sugarcane’ having the greatest value. FRAP ranged from 18.2 to 20.8 mg AAE/g DW at full-red maturity. All cultivars sampled from Alcalde in 2019 had a lower value FRAP on the last sampling date than on the first date (Table 2).
At Alcalde in 2019, there were no differences in FRAP levels on the last two harvest dates for ‘Lang’ and ‘Sugarcane’. The FRAP estimates ranged from 7.7 to 14.7 mg AAE/g DW on the last harvest date (11 Oct), when ‘Li’, ‘Lang’, and ‘Sugarcane’ were at full-red maturity. ‘Li’ and ‘Lang’ had a lower FRAP than ‘September Late’, which was not yet at full-red maturity. The FRAP value at both creamy and full-red maturity for each cultivar from Alcalde was greater in 2018 samples than 2019 (Fig. 3D).
Fruit sampled from Las Cruces in 2019 also showed a decreasing trend in FRAP across harvest dates (Table 3). Only the main effect of harvest date was significant (P < 0.05). FRAP least square means for ‘Li’, ‘Lang’, and ‘Sherwood’ were estimated to be 16.0, 14.9, and 17.2 mg AAE/g DW (SE = 0.52), respectively, with estimates of 25.8, 19.7, 10.5, and 8.3 mg AAE/g DW (SE = 0.54) across the harvest dates. Overall, FRAP values decreased across all harvest dates.
Los Lunas samples in 2019 also showed a decreasing trend in FRAP across harvest dates (Table 4). For fruit sampled on 30 Aug, when all cultivars were at the creamy stage, FRAP ranged from 14.7 to 24.9 mg AAE/g DW, and ‘Li’ had a greater FRAP value compared with other cultivars. FRAP ranged from 6.1 to 7.1 mg AAE/g DW on the last harvest date (27 Sep), when fruit were at full-red maturity, but there was no significant difference in FRAP among the cultivars studied.
Vitamin C contents were less at full-red maturity than at the creamy stage in jujube samples harvested from all sites and all cultivars (Tables 1–4, Fig. 3F). In 2018, on the last harvest date for each cultivar at Alcalde, NM, when all cultivars except ‘September Late’ were at full-red maturity, vitamin C ranged from 826.7 to 943.3 mg/100 g DW. Estimates at the creamy stage ranged from 910 to 1486.7 mg/100 g DW.
When vitamin C levels from 2018 and 2019 Alcalde samples were analyzed together, there was a significant year × cultivar interaction (P = 0.019). The main effect of maturity was significant. Overall, the vitamin C estimate was greater at the creamy stage compared with full-red maturity, with values of 1236.9 and 907.5 mg/100 g DW, respectively (SE = 39.75). In 2019, ‘Sugarcane’ had a greater vitamin C content than ‘Li’ and ‘Lang’, with average estimates of 1336.9, 913.7, and 975.9 mg/100 g DW, respectively.
For fruit sampled on 2 Aug 2019 at Las Cruces, when all cultivars were at the creamy stage, vitamin C levels ranged from 1592.5 to 2726.6 mg/100 g DW, and ‘Sherwood’ had a significantly greater vitamin C level compared with ‘Li’ and ‘Lang’. Jujubes sampled on 13 Sep, when all cultivars were at full-red maturity, had vitamin C contents ranging from 695.8 to 844.4 mg/100 g DW, without significant differences among cultivars tested.
At Los Lunas, there was no significant difference in vitamin C content for each cultivar on the last two harvest dates (13 Sep and 27 Sep), nor was there a significant difference in vitamin C among cultivars tested from creamy through full red (30 Aug to 27 Sep).
cAMP increased in the latter phase of maturity (Fig. 4). cAMP was not detected in ‘Lang’ and ‘Sugarcane’ samples from Alcalde in 2018 on the first harvest date (28 Aug). On the last harvest date when fruit of ‘Li’, ‘Lang’, and ‘Sugarcane’ were at full-red maturity, cAMP ranged from 66.5 to 189.2 µg/g DW. ‘Lang’ had the greatest value of cAMP, whereas ‘Sugarcane’ had the least cAMP. Late-cultivar September Late did not reach full-red maturity (Fig. 1), even by the last harvest date (9 Oct), because of the short growing season at Alcalde (Fig 4).
Citation: HortScience 58, 2; 10.21273/HORTSCI16880-22
In 2019, cAMP in ‘Li’, ‘Lang’, and ‘Sherwood’ samples increased significantly across the harvest dates at Las Cruces (Fig. 5). For each cultivar, there was no significant difference in cAMP between the first (2 Aug) and the second (16 Aug) harvest dates. Depending on the cultivar, cAMP ranged from 27.4 to 103.3 µg/g DW at the creamy stage (2 Aug), whereas at full-red maturity, cAMP ranged from 148.1 to 277.6 µg/g DW. At full-red maturity (13 Sep), ‘Sherwood’ had the greatest cAMP, followed by ‘Lang’ and ‘Li’ (Fig. 5).
Citation: HortScience 58, 2; 10.21273/HORTSCI16880-22
The Alcalde weather patterns were very different between 2018 and 2019. The long-term average (1953–2019) frost-free period is 146 d, and in the 10 years preceding the study was 150 d at Alcalde, NM (Yao et al. 2020). There were only 122 frost-free days in 2019, from 24 May to 23 Sept, which is 3 to 4 weeks shorter than average. The minimum daily temperatures from mid-May to early June were between 0 and 4.4 °C, much cooler than normal years, which greatly delayed fruit development and maturation. The frost that occurred on 23 Sep was also relatively early. Although it did not end the season, it affected fruit maturation. Fruit were forced to mature, and ‘September Late’ ended at the creamy stage in 2019 at Alcalde. Weather was relatively warmer in 2018, with more frost-free days than in 2019. Both minimum average monthly temperature and average monthly temperature from May to October were higher in 2018 than in 2019. The cool weather in 2019 affected Los Lunas but not Las Cruces. The cooler temperatures in Alcalde in 2019 could have affected the synthesis of phenolic compounds impacting TPC and PA content (Tables 1 and 2). Activity of phenylalanine ammonia-lyase, including other enzymes important in the phenolic biosynthetic pathway, is reported to be stimulated by the cold (Lattanzio 2013).
Each jujube tree blooms for 2 months or longer with its cyme inflorescence and flowers from current year shoots, resulting in differential fruit set. Consequently, fruit maturation on each tree lasts longer than most fruit species such as apple or peach (Yao 2018; Yao et al. 2020). In 2019, fruit from Las Cruces reached full-red maturity about 2 weeks earlier than Los Lunas and 4 weeks earlier than Alcalde. Fruit sampled on the same date were at different maturity depending on cultivar and location (Fig. 2). In 2019, the average fruit weight and TSS content in Alcalde samples were less than samples from Las Cruces and Los Lunas. Previous study has also shown better jujube fruit quality—fruit size, average fruit weight, and TSS—from southern locations compared with northern New Mexico (Yao et al. 2020).
Different studies have reported variation in nutrient profile and composition with locations (Chen et al. 2013; Sun et al. 2011). In 2019, for ‘Li’ and ‘Lang’, TPC estimates ranged from 10.6 to 11.4 (SE = 1.31), 10.9 to 12.9 (SE = 1.56), and 15.2 to 15.8 (SE = 1.19) mg GAE/g DW in samples from Las Cruces, Los Lunas, and Alcalde, respectively (Tables 2–4). PA estimates for ‘Li’ and ‘Lang’ ranged from 4.9 to 4.5 (SE = 1.36), 3.9 to 2.1 (SE = 1.89), and 5.3 to 1.9 (SE = 1.50) mg PA B2/g DW in samples from Las Cruces, Los Lunas, and Alcalde, respectively (Tables 2–4). Altitude differences among Alcalde (1737 m), Los Lunas (1480 m), and Las Cruces (1189 m), as well as climate, may have contributed to this variation because altitude and annual precipitation were demonstrated to affect the antioxidant levels in jujubes (Sun et al. 2011). As a plant matures, bioactive compounds are both synthesized and degraded (Guo et al. 2015). The colder temperatures in Alcalde accelerated fruit maturity and may have increased phenolic synthesis. It has been reported that the activity of the enzyme polyphenol oxidase, which degrades phenolic compounds and varies with season, temperature, pH, and substrate in various plants and food products (Lavelli and Caronni 2010; Thakur and Kapila 2017; Xu 2005).
Vitamin C content in plants can vary depending on environmental and developmental cues such as the photosynthetic process, relative humidity, oxidative stress, and temperature (Gomez and Lajolo 2008; Wang et al. 2014). As documented in ‘Kinnow’ mandarin and ‘Gunda Gundo’ orange, differences in jujube tree age among various locations could also be another factor affecting the synthesis of vitamin C (Aregay et al. 2021; Khalid et al. 2016). Because jujube trees at Alcalde, Los Lunas, and Las Cruces were planted in 2011, 2012, and 2017, respectively, tree age may affect the synthesis of different bioactive compounds and should be investigated in future studies.
In our study, two stages of edible maturity—creamy and full red—were identified visually based on the fruit’s peel color. Fruit designated as creamy had a creamy/yellowish peel, whereas full-red fruit had at least 95% red peel. As maturity increased, the amount of moisture, TPC, PAs, FRAP, and vitamin C decreased. This pattern is consistent with previous findings (Choi et al. 2012; Huang et al. 2017; Shi et al. 2018; Wang et al. 2016b; Xie et al. 2017). We measured overall phenolic content, although individual phenolic profiles and rates of degradation can vary with maturity (Choi et al. 2012; Shi et al. 2018). From creamy to full red, TPC fell by about 50% or a little more. The TPC value of immature fruit (until creamy) was roughly the same as that of PAs regardless of location and cultivar, which indicates that PAs may predominate in immature jujube fruit. cAMP increased at the latter stage of fruit maturity, consistent with other findings (Guo et al. 2015; Zhao et al. 2009). Depending on cultivar, location, and year, cAMP in our samples increased by 0.9 to 4.5 times from creamy to full-red maturity.
For common cultivars, depending on location, TPC, PAs, FRAP, and vitamin C in creamy fruit were, respectively, 1.0 to 1.8, 4.4 to 12.4, 1.9 to 2.6, and 0.1 to 1.3 times greater than that of fruit at full-red maturity. Therefore, jujube marketing, consumption, and processing of jujubes at the creamy stage will give the consumer greater potential health benefits.
Jujube extract can provide pharmacological benefits for the neurological and cardiovascular systems, and acts as an antioxidant and anticancer agent (Chen and Tsim 2020; Choi et al. 2012). The amount of energy, carbohydrate, protein, and fat in 100 g of fresh jujube is 79 kcal, 20.53 g, 1.2 g, and 0.2 g, respectively (Rashwan et al. 2020). Jujube cultivars tested in our study had substantial amounts of phenolics, vitamin C, and antioxidant capacity. Depending on the cultivar and location, TPC in jujube fruit at full-red maturity ranged from 10.6 to 16.8 mg GAE/g DW in our study, which is greater than the 5.18 to 7.42 mg GAE/g DW reported by Li et al. (2007). This variation may result from differences in cultivar, location, and drying technique. We used freeze-dried samples whereas Li et al. (2007) used sun-exposed air-dried samples. The jujube cultivars we examined had TPC levels several times greater relative to common fruit species, including apple (0.68 mg GAE/g DW), banana (0.57 mg GAE/g DW), cherry (1.15 mg GAE/g DW), red grape (0.80 mg GAE/g DW), plum (1.02 mg GAE/g DW), and pomegranate (1.47 mg GAE/g DW) (Huang et al. 2017). PAs also exhibit potential health benefits (Blade et al. 2016). PAs varied from 1.8 to 5.3 mg PA B2/g DW in our samples at full-red maturity, which is greater than the values reported by Chen et al. (2013). This could be the result of differences in cultivar/location in Chen et al. (2013). Our samples had PA concentrations that were comparable to the 1.0 to 4.1 mg of grape seed PA extract equivalent per gram of fresh weight reported in various cultivars (Gao et al. 2013).
Vitamin C is one of the three main components in jujube that exhibits antioxidant properties (Kou et al. 2015). The vitamin C concentration in our samples at full-red maturity ranged from 649.0 to 1153.3 mg/100 g DW, which has been observed to vary with cultivar. At full-red maturity, fruit of the cultivar Junzao had a vitamin C level of 1430 mg/100 g DW, comparable to our findings (Song et al. 2019). In a previous study at Alcalde between 2012 and 2015, vitamin C levels in 46 jujube cultivars ranged from 225 to 820 mg/100 FW (Huang et al. 2017). This corresponds to our result on a DW basis because vitamin C was concentrated in our samples of dried jujube powder. Jujube can be a great source of vitamin C, having a greater concentration than most vitamin C–rich fruit and vegetables, and this could be the reason why jujubes are called natural vitamin C pills (Huang et al. 2017).
The cyclic nucleotide cAMP is involved in the regulation of glycogen, sugar, and lipid metabolism (Kapalka 2009), and could possibly exhibit antiaging properties because exogenous cAMP improved aging-related phenotypes in mice (Wang et al. 2015). At ull-red maturity, cAMP in our samples ranged from 148.1 to 277.6 µg/g DW, which is comparable to other findings (Chen et al. 2013; Wang et al. 2016a). Potential health benefits of cAMP in jujube fruit can be obtained by consuming full-red jujubes.
In conclusion, consumption of jujube fruit at the creamy stage will render greater potential health benefits because creamy fruit have greater phenolics, antioxidant capacity, and vitamin C content compared with fruit at full-red maturity. Jujube fruit at full-red maturity can be a good natural source of cAMP, which is reported to have potential health benefits. Future studies on the dynamics of individual phenolic compounds, comparisons of nutrients in jujubes of similar age from different locations, and several years of study on climatic influences in nutrient content—especially in the northern part of New Mexico—are necessary to get better insight on this nutritious fruit. Limited parameters and cultivars were tested in this study, but jujube has a wide nutrient spectrum, including cAMP, vitamin C, antioxidants, flavonoids, polysaccharides, triterpenic acids, and so on. With recent advancements in metabolomics, we expect future research to explore this nutritious fruit and promote it to US consumers.
Fruit of jujube cultivars Li, Lang, Sugarcane, and September Late sampled from Alcalde, NM, at different harvest dates in 2018 and 2019. ND = no data.
Fruit of different jujube cultivars at different maturity sampled from Las Cruces (LC), Los Lunas (LL), and Alcalde (AL), NM, in 2019.
(A) Total phenolic content (TPC), (B) proanthocyanidins (PA), (C) antioxidant activity, (D) ferric reducing antioxidant potential (FRAP), (E) moisture, and (F) vitamin C in fruit of different jujube cultivars at creamy and full-red maturity harvested from Alcalde, NM, in 2018 and 2019. Different letters denote a significant difference at P < 0.05. AAE = ascorbic acid equivalent; DPPH = 2,2-diphenylpicrylhydrazyl; DW = dry weight.
Dynamics of cyclic adenosine monophosphate with maturity in different jujube cultivars harvested from Alcalde, NM, in 2018. Different lowercase letters for each cultivar denote a significant difference across harvest dates at P < 0.05. DW = dry weight.
Dynamics of cyclic adenosine monophosphate with maturity in different jujube cultivars harvested from Las Cruces, NM, in 2019. Different lowercase letters for each cultivar denote a significant difference across harvest dates at P < 0.05. Different uppercase letters at each harvest date indicate a significant difference among cultivars at P < 0.05
Contributor Notes
We thank Dr. Gill Giese and Frank Sholedice from New Mexico State University for their critical review of this manuscript before submission.
This project was supported in part by the Specialty Crop Block Grant through the New Mexico Department of Agriculture, Hatch funds from the United States Department of Agriculture National Institute of Food and Agriculture, and the New Mexico State University Agricultural Experiment Station.
S.Y. is the corresponding author. E-mail: yaos@nmsu.edu.
Fruit of jujube cultivars Li, Lang, Sugarcane, and September Late sampled from Alcalde, NM, at different harvest dates in 2018 and 2019. ND = no data.
Fruit of different jujube cultivars at different maturity sampled from Las Cruces (LC), Los Lunas (LL), and Alcalde (AL), NM, in 2019.
(A) Total phenolic content (TPC), (B) proanthocyanidins (PA), (C) antioxidant activity, (D) ferric reducing antioxidant potential (FRAP), (E) moisture, and (F) vitamin C in fruit of different jujube cultivars at creamy and full-red maturity harvested from Alcalde, NM, in 2018 and 2019. Different letters denote a significant difference at P < 0.05. AAE = ascorbic acid equivalent; DPPH = 2,2-diphenylpicrylhydrazyl; DW = dry weight.
Dynamics of cyclic adenosine monophosphate with maturity in different jujube cultivars harvested from Alcalde, NM, in 2018. Different lowercase letters for each cultivar denote a significant difference across harvest dates at P < 0.05. DW = dry weight.
Dynamics of cyclic adenosine monophosphate with maturity in different jujube cultivars harvested from Las Cruces, NM, in 2019. Different lowercase letters for each cultivar denote a significant difference across harvest dates at P < 0.05. Different uppercase letters at each harvest date indicate a significant difference among cultivars at P < 0.05
