Research Article

Desert Plant for Saline and Drought Stricken Farmland: Assessment of Opuntia cactus Nutritional Characteristics

Tiziana Centofanti1*, Gary Bañuelos2, Maria Clemencia Zambrano2 and Christopher M Wallis2

1Center for Irrigation Technology, California State University, Fresno, Fresno USA
2USDA, Agricultural Research Service, San Joaquin Valley Agricultural Sciences Center, South Riverbend Avenue, Parlier, USA

Received date: 14 Aug 2017; Accepted date: 31 Oct 2017; Published date: 08 Nov 2017.

*Corresponding author: Tiziana Centofanti, Center for Irrigation Technology, California State University, Fresno, Fresno, USA, Tel: +1-559-596-2885; E-mail: tiziana.centofanti@gmail.com
Abstract

Cactus pear is remarkable for its ability to tolerate arid saline environments that are recognized as stressful for most plant species. In addition, cactus pear can be cultivated with minimum agriculture inputs and thus has great potential for cultivation and production on degraded lands. In this three-year study, we assessed the physiological responses relative to nutraceutical quality in fruit juice extracted from fruit of Opuntia ficus-indica (USDA no. 248 and no. 255) that has been cultivated in saline, Se and B rich soils in the west side of the San Joaquin Valley in Central California.

Results indicate that the two selected accessions i.e., no.248 and no. 255, of Opuntia ficus-indica can well tolerate saline, Se and B impacted soils. Despite growing under high saline conditions the nutritional characteristics in fruit juice (as analyzed in this study, e.g., nutrients, total phenolics, ascorbic acid, pigments and flavonoids) of both accessions, were not affected by long-term (3 years) exposure to excessive salinity and B. In addition, juice extracted from fruits collected from plants grown on the saline, Se and B rich soil and drainage sediment showed significantly higher concentrations of Se relative to juice from fruits collected from plants grown on non-saline (control) soil. Keywords: Cactus Prickly Pear, Salinity, Selenium, Ascorbic Acid, Boron, Drought

Introduction

Cactus prickly pear (Opuntia ficus-indica (L. )Mill.) is native to the American Southwest and has been introduced in many other countries in the Mediterranean and western Pacific regions. The plant typically grows wild in desert and arid regions. The renewed interest in cultivation of cactus prickly pear can be ascribed to its multi-functionality as food, feed and medicinal and therapeutic uses [1]. Cactus prickly pear fruit is known to contain several useful chemical compounds that have desirable nutritional and medicinal properties, e.g., antixodants, phenolics, and vitamins [2].

Various commercial Opuntia clones have phenological, physiological and structural adaptations favoring survival in arid environments, in which water is the main factor limiting the development of most plant species [3]. Cactus pear is remarkable for its ability to tolerate arid saline environments that are recognized as stressful for most plant species [4]. In addition, cactus pear can be cultivated with minimum agriculture inputs and thus holds great potential for cultivation and production on degraded lands. In the west side of San Joaquin Valley (SJV) in Central California, soil salinization is a problem that threatens crop production [5]. Soils in the west side of the SJV were derived from Cretaceous shale rock and contain high levels of naturally occurring selenium (Se) oxyanions, sulfate, and boron (B) salts. In addition, Central California has been subject to recurrent severe drought from 2011 to 2015. Consequently, farmers in Central California are drilling more and deeper wells than ever before to pump water for the irrigation of their crops, fruit and nut orchards. Extensive drought causes economic losses for agriculturebased communities and is a threat to world food security. Hence, it is important that alternative solutions are identified and offered to famers in the west side of the SJV to prevent thousands of acres of farmland from going fallow due to excessive soil salinization and water scarcity. Agricultural strategies, such as identifying new seed varieties, irrigation technologies, and innovative agronomic practices, as well as accepting greater diversity of drought-tolerant crops, are needed to increase survival of farming in this part of California.

Opuntia ficus-indica may become an alternative crop that is well suited for cultivation in the arid growing conditions found in the west side of the SJV. In this regard, [4] We have selected accessions of Opuntia ficus-indica that were able to tolerate high salinity, Se and B levels present in drainage sediment collected from the San Luis Drain, near Mendota (CA). These authors documented the potential of Opuntia ficus-indica to tolerate growing in poor quality drainage sediment and to accumulate and gently volatilize Se and thereby reduce Se concentration in these sediments [6,7].

In this study, we assessed the physiological responses, relative to fruit nutraceutical quality extracted from fruit juice of Opuntia ficus-indica (USDA no. 248 and no. 255) that have been cultivated in saline, Se and B rich soils and drainage sediment for at least three years.

Opuntia ficus-indica(USDA no. 248) is potentially an attractive crop for farmers in the west side of the SJV because its dark purple fruit may have medicinal benefits, and importantly this accession (among many tested) tolerates drought, salt, and B, while accumulating and volatilizing Se [4].

Opuntia ficus-indica(USDA no. 255) produces red fruit but the accession appears to be most salt and B tolerant and produces fruit later than other accessions.

We measured the total phenolic concentration and composition of polyphenol compounds, color, pH, soluble solids, and concentration of mineral nutrients in whole fruit juice produced from fruit grown at three different field locations during 2012-2014, respectively.

Materials and Methods

Field sites

Three field sites (considered as treatments in the text) were used in this study containing the following: 1) a saline drainage sediment with high Se and B concentrations; 2) a saline, Se and B rich soil located at Red Rock Ranch, Five Points, CA; and 3) a non-saline sandy loam soil (control). The three sites were described as follows: 1) the saline rich drainage sediment with high Se and B concentrations was collected from the top 25-cm layer of residual sediment in the San Luis Drain, near Mendota, CA. The collected sediment was spread to a depth of 40 cm in an excavated field plot at the USDA Research Facility in Parlier, CA [8]. The drainage sediment was covered with a 4-cm layer of non-saline sandy loam soil to enhance biological activity, plant growth and survival;2) the saline field site at Red Rock Ranch was located at Five Points, CA, in the west side of the SJV. The soil is classified as an Oxalis silty clay loam (fine montmorillonitic, thermic PachicHaploxeral with a well-developed salinity profile). The soil contains naturally high concentrations of salts, e.g., Na2SO4, NaCl, CaCl2, Na2SeO4, CaSO4, Na2B4O5(OH)4, and CaB3O4(OH)3; and 3) the nonsaline sandy loam soil (control) located at the USDA Research Facility in Parlier CA is classified as a Hanford sandy loam (coarse-loamy, mixed, superactive, non-acid, thermic Typic Xerothents) field soil with a sand/ silt/clay distribution of 55%, 40%, and 5%, respectively. The non-saline control plots were prepared adjacent to the drainage sediment plots (field and plot description described later). See Table 1 for general soil chemical parameters at the respective growing sites. Normal agronomic management practices were applied on all test plots at all three field locations throughout each growing season, including applying a nonsulphur containing ammonium nitrate fertilizer at an application rate of 50 kg ⁄ha per year. All plots were drip-irrigated using a surface-drip irrigation system consisting of one in-line turbulent flow emitter per bed with an emitter spacing of 0.45 m and a flow rate of 4L⁄ h. The plants were irrigated with good quality water (electrical conductivity EC< 0.8 dSm-1) at the saline drainage sediment and the non-saline (control) plots. Irrigation was based on the rate of evapotranspiration (ET) losses recorded at the CIMIS weather station located 2 km away at the University of California (UC) Kearney Research Station in Parlier, CA. At the RRR field site, poor quality water (e.g., EC ranging 4-7 dS m-1, B and Se concentrations ranging 3-6 mg L-1 and 0.100-0.125 mg L-1, respectively) was applied with drip irrigation based on the rate of ET losses recorded at the CIMIS weather station at the UC west side Research Station located at Five Points, CA.

Selection, propagation, and plantation

Spineless prickly pear cactus (Opuntia ficus-indica (L.) Mill. accessions no. 248 and no. 255, were originally selected from individuals growing at the USDA–ARS National Arid Land Genetic Resources Unit in Parlier,CA, that originated in Mexico and Chile, respectively. Accessions no. 248 and no. 255 were selected for both their salt and B tolerance after growing for multiple growing seasons in agricultural drainage sediment [4], and importantly for the fruits’ red and purple colors [9]. Fruits of these colors have potentially higher economic value not only for their coloring potential as a source of natural colored compounds but also for their beneficial effects on consumers’ health as excellent source of dietary antioxidants. Both accessions were then clonally propagated, as described below.

For plant establishment, cladodes of both accessions were collected and propagated by placing an uprooted cladode (a stem segment) in soil. A lime/copper fungicide mixture was placed on the cut ends to prevent infections. The cladodes were then transplanted into pots containing the control sandy loam soil (see Table 1 for description of soil chemical characteristics). The cladodes were grown under natural growing conditions (200-400 μmol s-1 light intensity, temperature ranging from 17- 24 C, and 16/8 h light/dark period with circulated air) for 2 months within the greenhouse. Initially, the planted cladodes in the pots were grown without irrigation until new sprouts appeared for several weeks and then they were lightly watered with 1/5 strength Hoagland’s solution. After two months, when the new sprouts started appearing, the pots were placed outdoor at the USDA Research Facility in Parlier, CA, for 1 month. After 3 months of initial root establishment, the plants were transplanted into the saline drainage sediment, saline soil at RRR, and non-saline (control) sandy loam soil. Each 30m x 1m plot contained 10 plants spaced 1.2 m from each other and was replicated four times in different plots in the saline drainage sediment and three times in the non-saline soil.

Selection, propagation, and plantation

After three years of growth, the first fruit were handpicked from all plants in each plot at their respective growing site in 2012, 2013, and 2014. Fruit samples were washed and rinsed using DI water, dried with a paper towel, Ziploc bagged, and frozen at -20 C. Whole fruit were juiced using an electrical juicer (Hamilton Beach, Virginia, USA) that separates the peel, pulp and seeds from the juice.

In contrast to other studies [4,7], only the fruit juice was used for this study because the fruit collected from the plants grown on saline, B and Se rich soils are suitable for juice processing sold as fresh products for the market. The juice was stored in the freezer (-80 C) until analyses were performed, as described below.

Soluble solids, pH and color measurements in juice

Soluble solids (SS) content (Brix°) in fruit juice was determined using a digital refractometer (3810 PAL-1, Atago, Tokyo, Japan) and expressed as %. The pH was determined in fruit juice at room temperature using an Orion 420A pH meter (Thermo scientific, Waltham, USA). The color of fruit juice was determined using a Chroma Meter CR-400 optical sensor (Konica Minolta Sensing, Inc., Osaka, Japan) according to the CIE Lab [10]. The system provides the values of three color components; L∗, and the chromaticity coordinates, a∗ and b∗ [11].

Soil treatment

Total Se (μg g-1)

Water extractable Se

Water extractable B

Water extractable Na

EC (dS m-1)

pH

(μg mL-1)

(μg mL-1)

(μg mL-1)

RRR

4.0 (0.3)

0.2 (0.003)

10 (0.25)

1469 (0.2)

10 (0.6)

8.0 (0.06)

Sediment

1.8 (0.5)

0.9 (0.1)

5.9 (0.8)

525 (95)

4.8 (0.6)

7.9 (0.01)

Control

< 0.1 (0)

< 0.1 (0)

0.1 (0.01)

85 (17)

0.7 (0.1)

7.6 (0.01)

Table 1: Average total and extractable Se and other chemical parameters from 0 to 25 cm in various soil treatments (RRR = saline, Se and B rich soil at Red Rock Ranch, Sediment = saline drainage sediment plots, and Control = non-saline control soil). Data represent average of five replicates and standard error in brackets

Results were recorded as CIELAB values: L∗ (brightness), a* (redness), b* (yellowness), c* (chroma), and h* (hue). The instrument was calibrated using a standard white and a standard black reflective plate. Each color value reported is the mean of three determinations.

Water soluble mineral nutrients, electrical conductivity, and pH in soil

Water soluble nutrients concentrations (expressed as mg L-1), chloride, salinity [EC as dS m-1] and pH were determined in a 1:1 soil-water extract. Water soluble Se was analyzed using an Agilent ICP-MS (Santa Clara, CA) and the other soluble ions were measured using Varian Vista ICPOES (Palo Alto, CA) after preparing the samples, as described by [12]. Soil EC was measured at room temperature using an Orion Model 150 Conductivity Meter (Thermo Scientific, Waltham, USA), and pH was determined at room temperature using an Orion 420A pH meter (Thermo Scientific, Waltham, USA).

Water soluble mineral nutrients, electrical conductivity, and pH in soil

Water soluble nutrients concentrations (expressed as mg L-1), chloride, salinity [EC as dS m-1] and pH were determined in a 1:1 soil-water extract. Water soluble Se was analyzed using an Agilent ICP-MS (Santa Clara, CA) and the other soluble ions were measured using Varian Vista ICPOES (Palo Alto, CA) after preparing the samples, as described by [12]. Soil EC was measured at room temperature using an Orion Model 150 Conductivity Meter (Thermo Scientific, Waltham, USA), and pH was determined at room temperature using an Orion 420A pH meter (Thermo Scientific, Waltham, USA).

Total mineral nutrients

A standard procedure was used to determine the mineral element concentrations in juice samples [4]. Fruit juice samples were wet acid digested with HNO3-H2O2-HCl, as described by [13]. NIST coal fly ash (SRM 1633; Se content of 10.3 ± 0.6 mg kg-1, with a recovery of 93%) and NIST wheat flour (SRM 1567; Se content of 1.1 ± 0.2 mg kg-1, with a recovery of 94%) were used as an external quality control standards for the soil and plant material, respectively. Selenium and other elements were analyzed by an inductively-coupled plasma optical emission spectrometer (Agilent 7500cx, Santa Clara, USA) according to Agilent manufacture protocol.

Ascorbic acid

Ascorbic acid was quantified using a Shimadzu high-performance liquid chromatography (HPLC) device equipped with a Supelco C-610H ion-exchange column for separation. An isocratic flow of 0.1 mL/min 0.1% (v/v) phosphoric acid (from Sigma-Aldrich, St. Louis, MO) was used. Detection and quantification was made at 210 nm using a Shimadzu UV/Vis detector, with ascorbic acid standards (from Sigma) used for peak identification and to convert peak areas to gram amounts.

Total phenolics

Total phenolic concentrations were measured according to [14] using the Folin-Ciocalteu reagent assay. Absorbance was measured at 756 nm using a Spectra Max plus 384 spectrophotometer (Molecular Devices, Sunnydale, CA). Total phenols concentration were standardized against gallic acid (GA) and expressed as milligram of gallic acid equivalents (GAE) per L of fruit juice. The linearity range for this assay was determined as 50-250 mg L-1 GA, giving absorbance range of 0.5-2.55 AU.

Composition of polyphenols by liquid chromatography

The analysis of single phenolics was carried out to identify variation in specific compounds (pigments and polyphenols) because analysis of total phenolic comprises the bulk of all antioxidants and does not discriminate for single compounds. The Folin-Ciocalteu reagent also reacts with free phenylalanine and tyrosine, as well as proteins containing these amino acids.

In the juice samples, phenolic compounds were analyzed using a Shimadzu (Columbia, MD) high-performance liquid chromatography (HPLC) system equipped with a Shimadzu XR-ODS C18 column and a photodiode array detector (PDA) and weave lengths were set at 280 nm (for non-anthocyanins) and 520 nm (for betalains). A binary gradient was used, proceeding from 95% water (with 0.2% acetic acid) to 100% methanol (with 0.2% acetic acid) and back again over a 40 minute run time. All solvent reagents were obtained from Sigma [15]. Compounds were identified as previously described using a similar gradient and running on a HPLC equipped with a PDA to match UV/V is spectra andShimadzu LCMS-2020 mass spectrometer to derive molecular weights of quantified peaks [16,17,15]. In addition, standards of betanin and myricetin (obtained from Sigma) further confirmed identities of those compounds. Peak areas were converted to gram amounts using standard curves of quercetin-glucoside (from Sigma) for all flavonoid glycosides, and betanin for all betalains.

Statistical Analysis

Results were examined by factorial analysis of variance (ANOVA) with year, accessions, and growing location as main factors influencing the biochemical and quality parameters evaluated. Statistically significant differences were assumed for P ≤ 0.05 and calculated using Last Significance Differences comparison test. Statistical data analysis was performed using Gretl (Gnu Regression, Econometrics and Time-series Library) [18].

Results and Discussion

Fruit juice pH, soluble solids and color

Fruit produced from all growing locations were collected and evaluated to determine if any positive or negative responses were observed on nutritional quality in fruit juice when growing accessions no. 248 and no. 255 under poor growing soil conditions for at least three years. The following parameters were analyzed: fruit juice pH, soluble solids and color, mineral nutrients, ascorbic acid content, total phenolics, and polyphenols. Fruit juice pH ranged 4.7-5.7 (Table 2) and soluble solid values were significantly higher in 2013 for all treatments, and values were significantly lower in no. 248 and no. 255 in 2012 and in no. 248 in 2014 on saline soil at RRR. Juice pH measured in this study was similar to that reported by [19,20] in various clones of Opuntia ficus-indica from Mexico. Values of soluble solids ranged 9.3-14.0% (measure of maturity and related to sugar content) and were similar to the values reported by [21,20]. There were no significant differences in soluble solids concentrations among treatments and accessions.

Fruit of no. 248 are purple and fruit of no. 255 are red. Color values b* and c* were similar among treatments within the same accession indicating that the purity of the color were the same among treatments (Table 3). L*, h*, and a* values of the same accession were similar among treatments (Table 3). Differences in color values between accessions are attributed to the different color (purple no. 248 vs. red no. 255). The fruit color is of importance for consumers and absence of effect of treatment on fruit color is important to farmers. Red and purple fruit are considered to be the most desirable colors for prickly pear fruit and are the colors used by the natural dye industry [22].

Mineral nutrients

FConcentrations of mineral nutrients in fruit juice produced from all treatments are shown in Table 4 and Table 5. Irrespective of treatment, there were no significantly different concentrations of Ca, K, Cu, Mn, and Zn. Magnesium concentration in fruit juice was significantly higher in fruit juice collected in 2012 and 2014 from both accessions grown on the saline soil at RRR (Table 4). The concentration of P was significantly higher in fruit juice collected from plants grown on the non-saline (control) treatment (Table 4). Sulphur concentration was higher in fruit juice collected from both accessions grown on saline drainage sediment in 2013 and 2014 (Table 4). In this study, the highest concentrations of Ca and Mg were observed in fruit juice of plants grown on saline, Se and B rich soil at RRR (Table 4).

Except for no. 248 (in 2014), Na concentrations were always greater in saline treatments (Table 4). The soil at RRR and drainage sediment contain high concentrations of soluble Na that are readily taken up by the plants.

Iron concentration was significantly lower irrespective of growing site

Treatment1

Juice parameters

Year

248 Control

248 Sediment

248 RRR

255 Control

255 Sediment

255 RRR

Juice pH

2012

5.47 ± 0.36b

n.d.

5.00 ± 0.11c

n.d.

5.55 ± 0.12b

4.91 ± 0.07c

2013

5.60 ± 0.10a

5.67 ± 0.03a

5.68 ± 0.03a

5.84 ± 0.07a

5.77 ± 0.04a

5.42 ± 0.16b

2014

5.32 ± 0.06b

5.40 ± 0.06b

4.78 ± 0.07c

5.26 ± 0.07b

5.43 ± 0.03b

n.d.

Soluble solids (Brix, %)

2012

12.1 ± 0.35a

n.d.

9.37 ± 0.62ab

n.d.

9.33 ± 0.77ab

12.1 ± 0.35a

2013

12.5 ± 1.66a

13.5 ± 0.32a

13.6 ± 0.58a

14.0 ± 0.25a

13.7 ± 0.50a

12.9 ± 1.31a

2014

13.6 ± 1.29a

12.2 ± 0.48a

10.3 ± 0.58a

11.0 ± 0.33a

12.6 ± 0.49a

n.d.

Table 2: pH and soluble solids (SS, % Brix) measured in fruit juice of prickly pear cactus (accessions no. 248 and no. 255) grown in various soil treatment (RRR = saline, Se and B rich soil at Red Rock Ranch, Sediment = saline drainage sediment plots, and Control = non-saline control soil). Fruit were collected in 2012, 2013, and 2014. Data represent average ± standard error (n=3 or more than 3 depending on productivity (presence of fruit) for each replication in each year), respectively. Similar letters indicate no statistical (P ≤ 0.05) difference among treatments and all year for each juice parameters

Treatment1

Color parameters

Year

248 Control

248 Sediment

248 RRR

255 Control

255 Sediment

255 RRR

L*

2012

18.5 ± 2.02a2

n.d.

20.1 ± 1.90a

n.d.

25.8 ± 0.49a

28.0 ± 1.45a

2013

17.8 ± 0.29ab

18.2 ± 0.23a

21.7 ± 4.49a

27.9 ± 1.35a

28.9 ± 0.79a

28.2 ± 0.81a

2014

29.6 ± 11.7a

27.4 ± 7.30a

17.3 ± 0.49a

25.0 ± 0.61

27.6 ± 2.50a

n.d.

h

2012

13.9 ± 1.24b

n.d.

26.3 ± 10.2b

n.d.

68.3 ± 2.42a

75.0 ± 5.28a

2013

15.8 ± 1.67b

16.0 ± 0.60b

20.8 ± 5.85b

70.5 ± 4.34a

67.5 ± 1.29a

68.1 ± 4.48a

2014

28.9 ± 18.1b

39.2 ± 22.1b

9.0 ± 0.68b

10.1 ± 0.87b

13.9 ± 5.25b

n.d.

a*

2012

8.62 ± 1.06a

n.d.

8.62 ± 0.77a

n.d.

5.68 ± 0.74a

4.85 ± 1.68a

2013

14.6 ± 2.27a

15.0 ± 1.38a

10.4 ± 1.38a

6.14 ± 1.23a

9.21 ± 0.85a

7.22 ± 1.41a

2014

23.1 ± 19.2a

32.2 ± 22.3a

22.9 ± 0.24a

15.1 ± 0.75a

20.2 ± 5.05a

n.d.

b*

2012

2.16 ± 0.46b

n.d.

6.01 ± 3.19b

n.d.

14.2 ± 1.28a

18.3 ± 1.09a

2013

4.32 ± 1.03b

4.47 ± 0.57b

4.05 ± 1.07b

18.1 ± 1.19a

22.1 ± 1.51a

18.3 ± 1.22a

2014

11.3 ± 1.20b

8.92 ± 0.44b

9.26 ± 0.71b

18.4 ± 0.65a

17.5 ± 0.57a

n.d.

c*

2012

8.89 ± 1.14c

n.d.

11.8 ± 2.20c

n.d.

15.4 ± 1.34b

19.1 ± 0.89b

2013

15.3 ± 2.46c

15.6 ± 1.48c

11.8 ± 1.22c

19.4 ± 0.85b

24.0 ± 1.65b

20.1 ± 1.07b

2014

16.9 ± 4.30c

13.4 ± 0.56c

14.2 ± 0.57c

56.2 ± 3.00a

57.5 ± 2.64a

n.d.

Table 3: Color parameters (L*, a*, and b*) measured in fruit juice of prickly pear cactus (accessions no. 248 and no. 255) grown in various soil treatments(RRR = saline, Se and B rich soil at Red Rock Ranch, Sediment = saline drainage sediment plots, and Control = non-saline control soil). Fruit were collected in 2012, 2013, and 2014. Data represent average ± standard error (n=3 or more than 3 depending on productivity (presence of fruit) for each replication in each year), respectively. Similar letters indicate no statistical (P ≤ 0.05) difference among treatments and all years for each respective color

Treatment1

Nutrient

Year

248 Control

248 Sediment

248 RRR

255 Control

255 Sediment

255 RRR

Ca

2012

0.79 ± 0.48a2

n.d.

1.28 ± 0.33a

n.d.

0.82 ± 0.14a

1.59 ± 0.44a

2013

0.53 ± 0.07ab

0.59 ± 0.10ab

0.65 ± 0.13ab

0.69 ± 0.12ab

0.48 ± 0.09ab

0.58 ± 0.06ab

2014

0.51 ± 0.05a

0.79 ± 0.03a

1.08 ± 0.15a

0.57 ± 0.03a

0.67 ± 0.02a

n.d.

K

2012

1.95 ± 0.19a

n.d.

1.69 ± 0.14a

n.d.

2.19 ± 0.33a

2.33 ± 0.16a

2013

1.71 ± 0.06a

2.04 ± 0.25a

2.01 ± 0.18a

1.99 ± 0.10a

1.99 ± 0.23a

2.36 ± 0.19a

2014

1.71 ± 0.11a

1.90 ± 0.09a

1.84 ± 0.12a

1.61 ± 0.10a

2.01 ± 0.05a

n.d.

Mg

2012

0.45 ± 0.04b

n.d.

0.52 ± 0.07a

n.d.

0.29 ± 0.04b

0.59 ± 0.11a

2013

0.35 ± 0.04b

0.34 ± 0.06b

0.37 ± 0.05b

0.32 ± 0.06b

0.25 ± 0.03b

0.37 ± 0.01b

2014

0.25 ± 0.01b

0.24 ± 0.01b

0.52 ± 0.05a

0.33 ± 0.03b

0.22 ± 0.07b

n.d.

P

2012

0.19 ± 0.00a

n.d.

0.10 ± 0.01b

n.d.

0.11 ± 0.00b

0.13 ± 0.04b

2013

0.13 ± 0.02a

0.09 ± 0.01b

0.07 ± 0.01b

0.17 ± 0.02a

0.09 ± 0.01b

0.08 ± 0.01b

2014

0.18 ± 0.01a

0.11 ± 0.01b

0.07 ± 0.01b

0.15 ± 0.01a

0.12 ± 0.00b

n.d.

Na

2012

0.85 ± 0.56c

n.d.

0.90 ± 0.14b

n.d.

0.60 ± 0.06b

0.93 ± 0.30b

2013

0.23 ± 0.07c

0.60 ± 0.17c

1.13 ± 0.48b

0.59 ± 0.16c

0.38 ± 0.04b

1.18 ± 0.22b

2014

1.14 ± 0.20b

0.83 ± 0.12b

2.51 ± 0.41a

1.18 ± 0.29b

0.95 ± 0.12b

n.d.

S

2012

0.06 ± 0.00b

n.d.

0.12 ± 0.00b

n.d.

0.12 ± 0.01b

0.13 ± 0.01b

2013

0.06  ± 0.00b

0.99 ± 0.02a

0.09 ± 0.01b

0.10 ± 0.00b

0.79 ± 0.01a

0.09 ± 0.00b

2014

0.07 ± 0.00b

0.89 ± 0.00a

0.11 ± 0.01b

0.11 ± 0.00b

0.10 ± 0.00b

n.d.

Table 4:Concentrations of macro-nutrients (g L-1) detected in fruit juice of prickly pear cactus (accessions no. 248 and no. 255) grown in various soiltreatments (RRR = saline, Se and B rich soil at Red Rock Ranch, Sediment = saline drainage sediment plots, and Control = non-saline control soil). Fruit were collected in 2012, 2013, and 2014. Data represent average ± standard error (n=3 or more than 3 depending on productivity (presence of fruit) for each replication in each year), respectively. Similar letters indicate no statistical (P ≤ 0.05) difference among treatments and all years for each mineral nutrient

and accession in 2013 and 2014 (Table 5). Boron concentration was lower in fruit juice produced from plants grown non-saline (control) relative to the saline treatments at RRR and drainage sediment treatment (Table 5). Boron concentration was insignificantly higher in fruit of plants grown in drainage sediment, even though the amount of water extractable B in drainage sediment is lower than in the soil at RRR (Table 5).

Results of mineral elements measured in fruit juice from this study were comparable to those reported by [23,24] in cactus prickly pear and Myrtillocactus fruit, respectively. Fruit from Opuntia ficus-indica is characterized by high amounts of Ca (up to 0.59 mg kg-1) and Mg (0.98 mg kg-1) [3]. Among all the elements analyzed, Se concentrations were significantly higher in the fruit juice collected from plants grown on saline drainage sediment relative to the saline soil at RRR except for no. 255 in 2013 (Figure 1). Even though irrigation water contained selenium and other salts at RRR, the water contains high sulphate concentrations, which inhibits Se uptake from the soil into the plant. In contrast, the drainage sediment plot received good quality water and there was little inhibition of selenium uptake. Selenium concentrations were always significantly lower in fruit juice produced from plants grown on non-saline (control) treatments (Figure 1), where very little Se was present in the soil.

The Se concentrations reported in this study for fruit juice were lower than those reported by [4] for fruit skin and flesh of accession no. 248 (≈2 mg Se kg-1d.w.) grown on the same drainage sediment. [6] showed that most of the Se is stored in the seed and the pulp of the cactus fruit. Fruit of Opuntia ficus-indica have (been shown) to accumulate Se mostly as free seleno-cystathionine and Seleno-methionine [5]. Selenium is an essential micronutrient for humans and animals [6], and hence, drinking Se-enriched fruit juice may have extra health value for Se-deficient diets.

Ascorbic acid, total phenolic compounds, and polyphenols

Ascorbic acid in fruit juice ranged 0.8-1.7 mg mL-1, irrespective of treatment and accession (Figure 2). The lowest concentration of ascorbic acid was reported in fruit juice of no. 248 grown in the saline, Se and B rich soil at RRR. The values of ascorbic acid reported in this study for plants grown on saline, Se and B rich soil at RRR were, however, comparable to those reported by [25] in Opuntia ficus-indica fruit from Argentina.Concentrations of vitamin C in cactus pear fruit are higher than other common fruit such as apple, pear, grape, and banana [3].

In this study, the concentration of total phenolics ranged between 500 and 1000 mg GAE L-1 (Figure 3) and there were no significant differences for both accessions among treatments. Similar total phenolic concentrations were reported by [19] in fruit juice extracts from Opuntia ficus-indica.

These results from the fruit juice are one order of magnitude lower than those reported by [7,26,27] for whole fruit extracts of Opuntia ficus-indica. One possible explanation why no significant differences were observed among treatments for ascorbic acid, total phenolics, and polyphenols (see below) could be that all plants in the San Joaquin Valley (CA) suffered a recurrent historic drought (starting in 2010). Precipitation was extremely low during the growth cycle (April to October, below 1mm) and temperatures were very high (between 30 and >40 C) during the summer months. These climatic conditions may have overwhelmingly affected the productivity and nutritional quality of all plants, irrespective of growing site. Another plausible explanation is that the high salinity and B levels in the soil at RRR and in drainage sediment were not high enough to negatively affect ascorbic acid, total phenolics and/or polyphenols production.

Concentrations of pigments and flavonoids analyzed in fruit juice (Table 6) were generally similar (with few exceptions) among saline and non-saline (control) treatments for both accessions. No clear pattern was observed among growing sites and years for both accessions for all the polyphenols analyzed as shown in Table 6. It would be necessary to test the plants under a controlled environment to isolate multi-environmental factors that may have contributed to the variation of polyphenols concentrations in fruit juice observed in this field experiment.

Betanin, a betalain pigment, had the highest concentration in both accessions among all compounds analyzed (Table 6). These results are consistent with previous studies of betalain pigments of prickly pear cactus fruit [28,29,30].

Our data confirm the potential of prickly pear fruit juice as a source of natural healthy colorants that are rich in antioxidants and may provide protection against oxidative damage. Betanin is an antioxidant apparently

Treatment1

Nutrient

Year

248 Control

248 Sediment

248 RRR

255 Control

255 Sediment

255 RRR

B

2012

2.22 ± 0.11b2

n.d.

8.05 ± 2.02a

n.d.

14.0 ± 2.34a

10.3 ± 2.03a

2013

2.37 ± 0.35b

15.7 ± 2.7a

9.83 ± 1.96a

3.30 ± 1.00b

12.7 ± 1.58a

13.8 ± 2.71a

2014

2.76 ± 0.20b

12.5 ± 1.08a

10.0 ± 1.01a

3.30 ± 0.89b

9.61 ± 0.50a

n.d.

Cu

2012

0.84 ± 0.00a

n.d.

0.46 ± 0.08a

n.d.

0.43 ± 0.05a

0.43 ± 0.05a

2013

0.47 ± 0.05a

0.47 ± 0.05a

0.38 ± 0.07a

0.43 ± 0.02a

0.54 ± 0.15a

0.30 ± 0.03a

2014

0.41 ± 0.03a

0.40 ± 0.02a

0.44 ± 0.04a

0.35 ± 0.03a

0.29 ± 0.01a

n.d.

Fe

2012

1.91 ± 0.26a

n.d.

2.13 ± 0.62a

n.d.

2.74 ± 0.06a

1.98 ± 0.13a

2013

1.02 ± 0.12b

1.15 ± 0.10b

1.10 ± 0.25b

1.75 ± 0.34b

1.10 ± 0.14b

1.38 ± 0.22b

2014

0.92 ± 0.09b

1.26 ± 0.07b

1.29 ± 0.32b

1.45 ± 0.23b

1.48 ± 0.10b

n.d.

Mn

2012

8.95 ± 1.47a

n.d.

6.08 ± 1.81b

n.d.

3.95 ± 0.22bc

5.28 ± 0.72b

2013

3.73 ± 0.15c

2.91 ± 0.64c

3.09 ± 0.76c

6.42 ± 0.56b

3.18 ± 0.94c

3.25 ± 0.71c

2014

5.46 ± 0.69b

4.27 ± 0.39bc

3.57 ± 0.76c

5.78 ± 0.79b

3.22 ± 0.31c

n.d.

Zn

2012

1.24 ± 0.22a

n.d.

1.14 ± 0.24a

n.d.

0.88 ± 0.05a

0.99 ± 0.10a

2013

1.23 ± 0.15a

0.73 ± 0.06a

1.00 ± 0.19a

1.04 ± 0.04a

0.71± 0.06a

0.78 ± 0.04a

2014

1.28 ± 0.09a

0.88 ± 0.04a

0.87 ± 0.08a

1.00 ± 0.06a

0.80 ± 0.02a

n.d.

Table 5:Concentrations of micro-nutrients (mg L-1) detected in fruit juice of prickly pear cactus (accessions no. 248 and no. 255) grown in various soiltreatments (RRR = saline, Se and B rich soil at Red Rock Ranch, Sediment = saline drainage sediment plots, and Control = non-saline control soil). Fruitwere collected in 2012, 2013, and 2014. Data represent average ± standard error (n=3 or more than 3 depending on productivity (presence of fruit) for each replication in each year), respectively. Similar letters indicate no statistical (P ≤ 0.05) difference among treatments and all years for each nutrient

Treatment1

Polyphenols

Year

248 Control

248 Sediment

248 RRR

255 Control

255 Sediment

255 RRR

Indicaxanthin

2012

139 ± 10.0b2

n.d.

293 ± 42.7a

n.d.

184 ± 14.1ab

175 ± 19.7ab

2013

97.9 ± 6.80bc

182 ± 21.2ab

239 ± 48.5a

138 ± 8.65b

208 ± 45.2ab

178 v 41.8ab

2014

187 ± 24.0ab

185 ± 15.8ab

207 ± 55.6ab

226 ± 45.7ab

219 ± 30.6a

n.d.

Betanin

2012

6559 ± 229a

n.d.

5030 ± 950ab

n.d.

4593 ± 308ab

4110 ± 44.6b

2013

4617 ± 809ab

5091 ± 426ab

4060 ± 753b

5200 ± 477ab

5643 ± 549ab

6385 ± 1325a

2014

4530 ± 508ab

4970 ± 494ab

5223 ± 1088ab

4634 ± 560ab

3853 ± 455b

n.d.

Iso-betanin

2012

1718 ± 108ab

n.d.

1013 ± 125b

n.d.

1561 ± 156b

1014 ± 35.4b

2013

1113 ± 208b

1791 ± 277ab

2631 ± 517a

979 ± 110c

762 ± 44.6c

1031 ± 155b

2014

861 ± 133c

1863 ± 183ab

1951 ± 366b

851 ± 40.9c

798 ± 36.1c

n.d.

Gomphrenin

2012

1283 ± 31.2bc

n.d.

430 ± 85.5d

n.d.

1561 ± 156a

865 ± 198c

2013

776 ± 129c

1791 ± 277b

690 ± 136d

1040 ± 97.8bc

762 ± 44.6c

1125 ± 224bc

2014

939 ± 100c

1863 ± 183b

828 ± 146c

1122 ± 170bc

3853 ± 455a

n.d.

Diflavonoid glycoside

2012

237 ± 8.35c

n.d.

239 ± 73.6cd

n.d.

219 ± 15.7cd

255 ± 22.1c

2013

156 ± 10.2d

235 ± 21.3c

189 ± 38.7d

325 ± 14.9b

352 ± 22.3b

502 ± 31.8a

2014

267 ± 29.3c

192 ± 19.1d

320 ± 42.1a

299 ± 16.2b

287 ± 27.5bc

n.d.

Myricetinglucoside

2012

1141 ± 122b

n.d.

791 ± 273bc

n.d.

219 ± 15.7c

1210 ± 452b

2013

691 ± 53.3bc

253 ± 21.3c

594 ± 116bc

1220 ± 344b

352 ± 22.3c

2709 ± 382a

2014

1508 ± 216b

192 ± 19.1c

706 ± 162bc

2155 ± 311a

287 ± 27.5c

n.d.

Quercetage tintrimethyl glucoside

2012

182 ± 11.6c

n.d.

180 ± 78.9c

n.d.

234 ± 19.9c

263 ± 55.2c

2013

162 ± 18.8c

281 ± 35.1c

175 ± 33.8c

349 ± 14.7bc

419 ± 25.3b

656 ± 113b

2014

317 ± 39.4bc

188 ± 19.2c

233 ± 28.5c

366 ± 32.2bc

1280 ± 130a

n.d.

Flavonol-3-O-methyl ether

2012

157 ± 11.5bc

n.d.

96.4 ± 53.7c

n.d.

162 ± 16.0bc

102 ± 45.0c

2013

144 ± 10.9bc

202 ± 24.5b

152 ± 32.7bc

257 ± 21.2b

323 ± 37.6a

328 ± 38.6a

2014

237 ± 27.7b

138 ± 13.7bc

216 ± 32.1b

316 ± 25.1a

195 ± 21.1b

n.d.

Flavonoid glycoside 1

2012

133 ± 12.3bc

n.d.

89.5 ± 47.1c

n.d.

174 ± 15.5bc

49.0 ± 18.0c

2013

63.3 ± 6.35c

221 ± 23.8b

122 ± 26.8bc

211 ± 40.7b

327 ± 35.7a

332 ± 70.5a

2014

205 ± 23.3bc

159 ± 18.4bc

169 ± 45.1bc

237 ± 22.5b

164 ± 21.4bc

n.d.

Flavonoid glycoside 2

2012

332 ± 9.69b

n.d.

181 ± 80.5c

n.d.

307 ± 26.9b

457 ± 20.1b

2013

197 ± 141c

369 ± 54.5b

319 ± 60.0b

358 ± 93.1b

328 ± 50.3b

857 ± 176a

2014

367 ± 48.2b

254 ± 29.2bc

349 ± 61.1b

478 ± 93.7b

403 ± 32.8b

n.d.

Isorhamnetin-glucosyl-rhamnosyl-rhamnoside

2012

732 ± 55.3b

n.d.

512 ± 358c

n.d.

688 ± 65.0c

867 ± 248b

2013

346 ± 2.49c

692 ± 100b

533 ± 108c

836 ± 89.3b

973 ± 92.8b

1397 ± 96.5a

2014

915 ± 124a

678 ± 55.3b

1062 ± 167ab

1368 ± 166a

999 ± 108b

n.d.

Isorhamnetin-rhamnosyl-rhamnosyl-rhamnoside

2012

143 ± 21.5c

n.d.

237 ± 178bc

n.d.

193 ± 24.6bc

267 ± 63.0b

2013

49.8 ± 1.64d

195 ± 34.bc

150 ± 32.9c

286 ± 40.6b

341 ± 44.9b

743 ± 83.3a

2014

307 ± 44.6b

156 ± 18.9c

291 ± 53.8b

480 ± 86.9b

316 ± 47.9b

n.d.

Isorhamnetin glucosyl rhamnoside

2012

328 ± 154b

n.d.

164 ± 111c

n.d.

163 ± 25.3c

53.6 ± 0.39d

2013

270 ± 153b

174 ± 25.7c

285 ± 61.8b

380 ± 98.2b

383 ± 61.4b

760 ± 105a

2014

293 ± 60.7b

125 ± 9.24c

277 ± 37.7b

379 ± 237b

68.7 ± 10.1d

n.d.

Table 6:Concentration of polyphenols (μg g-1f.w.) detected in fruit juice of prickly pear cactus (accessions no. 248 and no. 255) grown in various soil treatment (RRR = saline, Se and B rich soil at Red Rock Ranch, Sediment = saline drainage sediment plots, and Control = non-saline control soil). Fruit were collected in 2012, 2013, and 2014. Data represent average ± standard error (n=3 or more than 3 depending on productivity (presence of fruit) for each replication in each year), respectively. Similar letters indicate no statistical (P ≤ 0.05) difference among treatments and all years for each polyphenols

involved in a number of model systems of lipid oxidation. [31] found that very small concentrations of betanin, extracted from red beet, inhibited lipid peroxidation and hemede composition. The authors concluded that inclusion of betanin-rich foods (i.e., red beet) in the diet might provide protection against certain oxidative stress-related disorders in humans.

Betalain is a widely used natural colorant in the food industry and betalains for food use are extracted from red beet (Beta vulgaris L.). However, the high concentrations of betalain found in fruit juice from Opuntia ficusindica in this study make it an even better source of betalains than red beet [3].

Most flavonoid concentrations reported in this study (Table 6) are in the range 100- 600 mg g-1 and are comparable to data reported by [26] in fruit juice of Opuntia ficus-indica.

Conclusions

Overall, our study indicates that the two selected accessions no.248 and no. 255 of Opuntia ficus-indica can be grown under high saline, B, and drought conditions and their nutritional characteristics in fruit juice (as analyzed in this study e.g., nutrients, total phenolics, ascorbic acids and pigments, and flavonoids) are not affected by adverse growing conditions.

Figure 1: Selenium concentrations in fruit juice of prickly pear cactus (accessions no. 248 and no. 255) grown in various soils (RRR = saline, Se and B rich soil at Red Rock Ranch, Sed = saline drainage sediment plots, and control = non-saline control soil).Fruit were collected in 2012, 2013, and 2014. Bars and error bars represent average and standard error (n=3 or more than 3 depending on productivity (presence of fruit) for each replication in each year), respectively. Treatment 248 control consists of n=2. Similar letters indicate no statistical (P ≤ 0.05) difference among treatments and all years
Figure 2: Ascorbic acid in fruit juice of prickly pear cactus (accessions no. 248 and no. 255) grown in various soils (RRR = saline, Se and B rich soil at Red Rock Ranch, Sediment = saline drainage sediment plots, and Control = non-saline control soil). Fruit were collected in 2012, 2013, and 2014. Bars and error bars represent average and standard error (n=3 or more than 3 depending on productivity (presence of fruit) for each replication in each year), respectively. Treatment 248 control consists of n=2. Similar letters indicate no statistical (P ≤ 0.05) difference among treatments; when no letters are present then there were no significant differences among treatments and all years
Figure 3: Concentration of total phenolics in fruit juice of prickly pear cactus (accessions no. 248 and no. 255) grown in various (RRR = saline, Se and B rich soil at Red Rock Ranch, Sediment = saline drainage sediment plots, and Control = non-saline control soil).Fruit were collected in 2012, 2013, and 2014. Bars and error bars represent average and standard error (n=3 or more than 3 depending on productivity (presence of fruit) for each replication in each year), respectively. Treatment 248 control consists of n=2. Similar letters indicate no statistical (P ≤ 0.05) difference among treatments; when no letters are present then there were no significant differences among treatments and all years

In addition to no adverse effect observed on the nutritional quality of fruit juice produced on poor quality soil and drainage sediment, fruit juice produced from plants grown on the saline, Se and B rich soil and drainage sediment showed significantly higher concentrations of Se relative to fruit juice of plants collected on non-saline (control) soil.

Acknowledgments

We would like to thank Ms. Teagan Zoldoske, Ms. Anna Allen and Mr. Justin King for their assistance during field and laboratory operations. In addition, a special thank you to Mr. Irvin Arroyo for his invaluable analytical and technical contribution to this study. Financial support was provided by California Department of Water Resources Proposition 204 and California State University Fresno Agriculture Research Initiative.

Disclaimer

Mention of specific products is for identification and does not imply endorsement by the US Department of Agriculture to the exclusion of other suitable products or suppliers.

Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.

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