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Shiow Y. Wang and Kim S. Lewers

Fruit of the cultivated strawberry (Fragaria ×ananassa Duchesne ex Rozier) are a good source of natural antioxidants, which play an important role in protecting human health. Antioxidant levels vary considerably among strawberry genotypes. The cultivated strawberry is a hybrid of two very different wild progenitor species: F. virginiana Mill. and F. chiloensis (L.) Mill. The progenitor species are valued by strawberry breeders as sources of novel traits, but have not been evaluated for antioxidant capacity or levels of antioxidant compounds. The objectives of this study are 1) to evaluate the antioxidant contents and antioxidant activities in representatives of F. virginiana and F. chiloensis in comparison with representatives of the cultivated strawberry species (F. ×ananassa), 2) to determine which strawberry compounds are most closely correlated with antioxidant capacity among these three species, and 3) to identify wild strawberry genotypes with high antioxidant activity and bioactive compounds for use in cultivar development. Fruit of 19 accessions from each of the three species, cultivated strawberry plus the two progenitor species (F. ×ananassa, F. virginiana, and F. chiloensis), were evaluated for levels of antioxidant capacity (oxygen radical absorbance capacity), total phenolics, total anthocyanins, ellagic acid, quercetin 3-glucoside plus quercetin 3-glucuronide, kaempferol 3-glucoside, kaempferol 3-rutinoside, p-coumaryl–glucose, pelargonidin 3-glucoside, pelargonidin 3-glucoside–succinate, cyanidin 3-glucoside, and cyanidin 3-glucoside–succinate. Fruit of the 13 accessions tested from the wild progenitor species F. virginiana had significantly higher antioxidant capacity, total phenolics, and total anthocyanins than did the fruit of three accessions tested from the cultivated strawberry F. ×ananassa, or the three accessions tested from the other wild progenitor species (F. chiloensis), and will be valuable as a source of parent material for developing more nutritious strawberry cultivars. The high correlation with antioxidant capacity, relative efficiency, and lack of genotype-by-year interaction in this study suggests that the measurement of total phenolics may be the better assay to use for the later selection stages in a strawberry cultivar development program. Of the evaluated F. virginiana accessions, NC 95-19-1, JP 95-1-1, CFRA 0982, NC 96-5-3, and RH 30 fruit were highest in antioxidant capacity and should prove useful toward development of strawberry cultivars with high antioxidant capacities.

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Shiow Y. Wang and Hsin-Shan Lin

Fruit and leaves from different cultivars of thornless blackberry (Rubus sp.), red raspberry (Rubus idaeus L.), black raspberry (Rubus occidentalis L.), and strawberry (Fragaria × ananassa D.) plants were analyzed for total antioxidant capacity (oxygen radical absorbance capacity, ORAC) and total phenolic content. In addition, fruit were analyzed for total anthocyanin content. Compared to fruit, leaves were found to have higher ORAC values. In fruit, ORAC values ranged from 7.8 to 33.7 μmol Trolox equivalents (TE)/g of fresh berries, while in leaves, ORAC values ranged from 20.8 to 45.6 μmol TE/g of fresh leaves. Fruit harvested at different stages of maturity were analyzed in blackberries, raspberries, and strawberries. Blackberries and strawberries had their highest ORAC values during the green stages, while raspberries generally had the highest ORAC activity at the ripe stage (with exception of cv. Jewel, a black raspberry). Total anthocyanin content increased with maturity for all three fruit. There was a linear correlation existed between total phenolic content and ORAC activity for fruit and leaves. For ripe berries, there was also a linear relationship between ORAC values and anthocyanin content. Of the ripe fruit and leaves tested, raspberry plants appeared to be the richest source for antioxidants.

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Shiow Y. Wang and Gene J. Galletta

The effect of silicon (Si) foliar applications on metabolic changes and powdery mildew infection in strawberry plants were determined. Silicon was used in the forms of potassium (K) and sodium (Na) salts. Foliar sprays containing 0, 250, 500, 750, and 1000 ppm of Si were applied. Strawberry plants showed no difference in response to the K or Na salts of Si during the seven weeks of experimental period. Plants treated with potassium and sodium silicate showed reduced severity of powdery mildew, increased chlorophyll content, and increased plant growth. Potassium and sodium silicate treatments also induced metabolic changes such as an increase in citric acid and malic acid levels, and a decrease in fructose, glucose, sucrose, and myoinositol content. The treated tissues also had higher ratios of (18:2 + 18:3)/18:1 in glycolipids and phospholipids and elevated amounts of membrane lipids in leaves and petioles. These results suggest that Si has beneficial effects on strawberry plants and may serve as an alternative to fungicides for controlling powdery mildew.

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Shiow Y. Wang, Gene J. Galletta, and John L. Maas

Fruit quality of 24 selected strawberry cultivars and selections were evaluated. There were great variations in the contents of soluble solids, titratable acidity, carbohydrates, organic acids, and ascorbic acid among different cultivars, reflecting primary genetic differences. Fructose, glucose, and sucrose were found to be the three major sugars, comprising >65% of the total soluble solids in strawberry. Fruit contained lower sucrose compared to fructose and glucose, whereas leaves contained comparable amounts of fructose, glucose, and sucrose. Citric acid was the major organic acid in strawberries. Strawberries were also rich in ascorbic acid. Leaves were much higher in ascorbic acid than fruit. There appeared to be no correlation between fruit and leaves on carbohydrate, organic acid, and ascorbic acid contents.

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Shiow Y. Wang, Miklos Faust, and Michael J. Line

The effect of IAA on apical dominance in apple buds was examined in relation to changes in proton density (free water) and membrane lipid composition in lateral buds. Decapitation induced budbreak and enhanced lateral bud growth. IAA replaced apical control of lateral buds and maintained paradormancy. Maximal inhibition was obtained when IAA was applied immediately after the apical bud was removed; delaying application reduced the effect of IAA. An increase in proton density in lateral buds was observed 2 days after decapitation, whereas the change in membrane lipid composition occurred 4 days later. Removing the terminal bud increased membrane galacto- and phospholipids and the ratio of unsaturated to corresponding saturated fatty acids. Decapitation also decreased the ratio of free sterols to phospholipids in lateral buds. Applying thidiazuron to lateral buds of decapitated shoots enhanced these effects, whereas applying IAA to the terminal end of decapitated shoots inhibited the increase of proton density and prevented changes in membrane lipid composition in lateral buds. These results suggest that change in water movement alters membrane lipid composition and then induces lateral bud growth. IAA, presumably produced by the terminal bud, restricts the movement of water to lateral buds and inhibits their growth in apple.

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Shiow Y. Wang, Dean Der-Syh Tzeng, and Gene J. Galletta

Foliar application of a mixture of methionine and riboflavin was effective in reducing the severity of powdery mildew [Sphaerotheca macularia (Wallr. ex Fr.) Jacz. F. sp. Fragariae] infection in 72 strawberry progenies and over 110 clonal genotypes. This biocidal activity was enhanced by supplement of copper, iron, and surfactants [such as sodium dodecyl sulfate (SDS), Triton X-100, or Tween-20]. Compounds free radical scavengers (n-propyl gallate, thiourea), or antioxidants (α-tocopherol, -carotene) reduced its biocidal activity. Plants treated with the MR formulation (26.6 μM riboflavin, 1 mM D,L-methionine, 1 mM copper sulfate pentahydrate and 1 mg·ml–1 SDS) or 29% SP formulation of MR (Technical Division of the American Cyanamid Corporation, Taiwan Subsidiary at Taipei) not only showed decreased powdery mildew infection but also showed increased chlorophyll content and leaf area and improved fruit quality. Results in this study suggest that treatment with mixture of methionine and riboflavin is beneficial to strawberry plants and may serve as an alternative to fungicides for controlling powdery mildew.

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Shiow Y. Wang, Miklos Faust, and Michael J. Line

The effect of Indole-3-acetic acid (IAA) on apical dominance in apple (Malus domestica Borkh.) buds was examined by studying changes In proton density (free water) and membrane lipid composition in lateral buds. Decapitation induced budbreak and enhanced lateral bud growth. IAA replaced apical control of lateral bud paradormancy. Maximal inhibition was obtained when IAA was applied immediately after the apical bud was removed. Delaying this application weakens the effect of IAA. An increase in proton density in lateral buds was observable 2 days after decapitation, whereas the change in membrane lipid composition occurred 4 days later. Decapitating the terminal bud induced an increase in membrane galacto- and phospholipids. and the ratio of unsaturated to corresponding saturated fatty acids. Decapitation also induced a decrease in the ratio of free sterols to phospholipids in lateral buds. Application of IAA to the terminal end of decapitated shoots inhibited the increase of proton density and prevented changes in the membrane lipid composition of lateral buds.

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Shiow Y. Wang, Hong J. Jiao, and Miklos Faust

The activity of glucose-6-phosphate dehydrogenase (G6PDH), 6-phosphate gluconate dehydrogenase (6PGDH), isocitrate dehydrogenase (ICDH), pyruvate kinase (PK), and glyceraldehyde-3-phosphate dehydrogenase (GAPDH) were studied in apple (Malus domestics Borkh.) buds during dormancy and thidiazuron-induced budbreak. When buds were dormant, the activity of the glycolytic enzymes GAPDH and PK and the tricarboxylic acid (TCA) cycle enzyme ICDH was low compared to that in nondormant buds. The activity of these enzymes increased during budbreak, peaked when buds were in the green tip stage just before the start of rapid expansion (at 8 days after thidiazuron treatment), and declined thereafter. The activity of pentose-phosphate cycle enzymes G6PDH and 6PGDH was higher in dormant buds than in nondormant buds. 6PGDH was about twice as high as G6PDH. During budbreak and resumption of growth, G6PDH and 6PGDH activity decreased.

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John L. Maas, Shiow Y. Wang, and Gene J. Galletta

Ellagic acid in tissue extracts of green and red-ripe strawberries (Fragaria × ananassa Duch.) was detected and quantified by HPLC. Ellagic acid content of green fruit pulp ranged from 1.32 to 8.43 mg·g-1 of tissue dry weight (mean 3.36 mg·g-l) and in achenes of green fruit from 1.32 to 20.73 mg·g-1 (mean 7.24). Ellagic acid content of red fruit pulp at one location for 35 cultivars and selections ranged from 0.43 to 4.64 mg·g-1 of dry weight (mean 1.55) and from 0.43 to 3.47 mg·g-l (mean 1.45) for 15 clones at another location. Achenes from red-ripe fruit ranged from 1.37 to 21.65 mg·g-1 (mean 8.46) for 34 clones at one location and from 2.81 to 18.37 mg·g-1 (mean 8.93) for 15 clones at another location. Leaf ellagic acid content ranged from 8.08 to 32.30 mg·g-1 of dry weight (mean 14.71) for 13 clones examined. Large differences in ellagic acid content were found among cultivars, but tissue values were not consistent within cultivars. Values from one tissue type did not correlate consistently with values of the other tissues. Sufficient variation was found among cultivars to suggest that increased ellagic acid levels may be achieved in progeny from crosses with selected parental material.

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Shiow Y. Wang, Kim S. Lewers, Linda Bowman, and Min Ding

Fruit extracts from 17 to 18 representatives of three strawberry species [Fragaria virginiana Mill., F. chiloensis (L.) Mill., and F. ×ananassa Duchesne ex Rozier] were tested for the ability to inhibit proliferation of A549 human lung epithelial cancer cells. The fruit extracts also were tested for activities against free radicals, (peroxyl radicals, hydroxyl radicals, singlet oxygen, and superoxide radicals), the activities of antioxidant enzymes [glutathione peroxidase (EC 1.11.1.9), superoxide dismutase (EC 1.15.1.1), guaiacol peroxidase (EC 1.11.1.7), ascorbate peroxidase (EC 1.11.1.11), monodehydroascorbate reductase (EC 1.6.5.4), dehydroascorbate reductase (EC 1.8.5.1), and glutathione reductase (EC 1.6.4.2)], and the activities of nonenzyme antioxidant components, ascorbic acid and glutathione. Correlations between the proliferation of cancer cells and these antioxidant activities were calculated. At the species level, F. virginiana fruit extract inhibited the proliferation of A549 human lung epithelial cancer cells to a significantly greater extent (34% inhibition) than the extracts from fruit of either F. chiloensis (26%) or F. ×ananassa (25%) (P < 0.0001). Extracts from fruit of F. virginiana also had significantly greater antioxidant activities and higher activities of antioxidant enzymes and nonenzyme components than did extracts from the other two species. Among individual genotypes, there was a high positive correlation between antiproliferation of A549 cancer cells, antioxidant activities against free radicals, activities of antioxidant enzymes, and activities of nonenzyme components. Although all fruit extracts from all the strawberry genotypes inhibited proliferation of A594 cancer cells, fruit extracts from seven F. virginiana genotypes showed significantly greater antiproliferative effects than any of the F. ×ananassa or F. chiloensis genotypes. These genotypes, CFRA 0982, JP 95-1-1, NC 95-19–1, RH 30, NC 96-48-1, JP 95-9-6, and LH 50-4, may be especially useful in developing cultivars with greater anticancer potential.