The genotypic effects on the chemical composition and antioxidant activity of sea buckthorn (Hippophae rhamnoides L.) berries grown in Turkey

Scientia Horticulturae 115 (2007) 27–33 www.elsevier.com/locate/scihorti

The genotypic effects on the chemical composition and antioxidant activity of sea buckthorn (Hippophae rhamnoides L.) berries grown in Turkey Sezai Ercisli a,*, Emine Orhan a, Ozlem Ozdemir a, Memnune Sengul b b

a Department of Horticulture, Faculty of Agriculture, Ataturk University, 25240 Erzurum, Turkey Department of Food Engineering, Faculty of Agriculture, Ataturk University, 25240 Erzurum, Turkey

Received 8 May 2007; received in revised form 9 July 2007; accepted 11 July 2007

Abstract In this study, chemical composition of berries of 10 sea buckthorn (Hippophae rhamnoides L.) genotypes in Turkey was investigated. The total phenolic content of the berries ranged from 21.31 mg gallic acid equivalents (GAE) per g dry weight basis to 55.38 mg GAE per g. The highest antioxidant activity was 93.54% (similar to the standard BHT at 200 mg/L) and the lowest was 80.38%. There was no correlation (R = 0.688) between the total phenolic content and the antioxidant activity. The major fatty acids in berries were palmitoleic acid (35.48%), followed by palmitic acid (28.13%), oleic acid (22.89%) and linoleic acid (3.96%). Total soluble solid content of sea buckthorn genotypes varied from 10.15 to 14.80%, titratable acidity varied from 2.64 to 4.54%, the pH varied from 2.63 to 2.98 and Vitamin C varied from 19 to 121 mg/100 mL. The average content of minerals in the sea buckthorn berries of different genotypes was 20,800 ppm N, 7100 ppm P, 7260 ppm K, 1960 ppm Ca, 1465 ppm Mg, 32 ppm Zn, 24 ppm Cu, 22 ppm Mn and 7 ppm Fe. # 2007 Elsevier B.V. All rights reserved. Keywords: Hippophae rhamnoides; Chemical composition; Genotypic effect

1. Introduction Epidemiological studies suggest that a diet, that includes vegetables and fruits, may reduce risk of certain types of human cancer (Meyskens and Szabo, 2005). Among colored fruits, berries such as blackberry (Rubus sp.), black raspberry (Rubus occidentalis), blueberry (Vaccinium corymbosum), cranberry (Vaccinium macrocarpon), black mulberry (Morus nigra), red raspberry (Rubus idaeus) and strawberry (Fragaria  ananassa) are consumed both in fresh and in processed forms. In addition, berry extracts are widely consumed as dietary supplements for their potential human health benefits (Robards et al., 1999). The health benefits of berries may be partly attributed to their high content of phenolic compounds, as phenolics possess a wide spectrum of biochemical activities such as antioxidant, antimutagenic, anticarcinogenic, as well as their abilities to modify gene expression (Nakamura et al., 2003).

* Corresponding author. Tel.: +90 442 2312599; fax: +90 442 2360958. E-mail address: [email protected] (S. Ercisli). 0304-4238/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.scienta.2007.07.004

Sea buckthorn (Hippophae rhamnoides L.) is a winter hardy, drought resistant deciduous shrub with yellow or orange berries (Sabir et al., 2003). It develops an extensive root system rapidly and is therefore an ideal plant for preventing soil erosion and land reclamation, and it withstands temperatures from 43 to 40 8C (Lu, 1992). The berries of sea buckthorn can be used for many purposes and have a large economic potential. The berries have been used for centuries in Europe and Asia. Recently, sea buckthorn has attracted considerable attention from researchers around the world mainly for its nutritional and medicinal value. The berries have a high content of bioactive compounds and are rich in carbohydrates, protein, fatty acids, organic acids, amino acids and vitamins (Yao and Tigerstedt, 1992; Guliyeva et al., 2004; Sabir et al., 2005a; Tiitinen et al., 2005). The concentration of Vitamin C in sea buckthorn berries ranged from 28 to 310 mg/ 100 g (Yao and Tigerstedt, 1992) and is higher compared to other berries such as strawberry, raspberry and blackberry. In addition to the medicinal use, the berries of sea buckthorn can be processed to juice and jam, or be used as flavoring in dairy products because of their unique taste. In Turkey, sea buckthorn is widely distributed throughout North and East Anatolia and known locally as ‘‘Yalancı igde’’

28

S. Ercisli et al. / Scientia Horticulturae 115 (2007) 27–33

or ‘‘Karga dikeni’’ (Baytop, 1999; Cakir, 2004). Cultivating sea buckthorn in Turkey is encouraged by the local people who can obtain an income by harvesting the berries. Published literature suggests that a substantial part of the geographic variation in physiochemical characteristics of sea buckthorn berries is associated with the genotypes in local populations. Analysis of compounds in berries of different sea buckthorn genotypes could therefore result in useful information for further breeding studies. Several studies on physiochemical compounds of sea buckthorn berries have been published in Finland (Tiitinen et al., 2005), Sweden (Gao et al., 2000), Poland (Kawecki et al., 2004), Pakistan (Sabir et al., 2005a), India (Ranjith et al., 2006) and China (Tong et al., 1989). On the other hands, few reports have dealt with the total anthocyanins, total phenolics and fatty acids. To our knowledge, there have been only one report on fatty acid composition of sea buckthorn berries in Turkey (Cakir, 2004). No detailed comparative reports have been published on physiochemical composition of different sea buckthorn genotypes naturally grown in Turkey especially of sea buckthorn growing area in Coruh Valley which has a unique geoclimatic conditions of high altitude coupled with extreme variations in temperature (20 to 35 8C). 2. Material and methods 2.1. Collection and preparation of berry samples Sea buckthorn berries from the selected genotypes ESB-1 (ESB: Erzurum Sea Buckthorn) to ESB-10 were harvested same exact plants in both 2005 and 2006 years. The harvest time of genotypes was different and it was estimated to be a reasonable time for commercial harvesting for all genotypes. Before the last week of August the berries were unpalatable and after the first week of September the berries started to be difficult to harvest due to loss in firmness in both years. The plants were found as wild in single location, Uzundere town (latitude 408330 N, longitude 418350 E and altitude 1025 m) in Coruh Valley in Turkey. These genotypes were previously selected according to selection criterion such as high yield, free of diseases and pests, fruit juice ratio, easy to harvest and total soluble solid contents. Among genotypes, the berries from ESB-1 and ESB-2 harvested very easily. The leaf areas of genotypes were between 1.72 cm2 (ESB-9) and 3.81 cm2 (ESB-5). The genotypes of ESB-6 and ESB-8 had dwarf growth habit. There were no statistical significant differences in the profiles and yields of the different phytochemicals being analyzed between the 2 years, therefore the data of the different years were pooled (this could be a consequence of similar growing and climatic conditions in both years in the area where the plants grow). Approximately, 500 berries were collected from different branches of plants. Half of the amount of harvested berries was processed immediately for analysis of soluble solids (determined as Brix), pH, Vitamin C, anthocyanin, acidity and antioxidant activity, whereas the rest of the berries were stored at 20 8C

before analysis of oil, fatty acids and minerals. Seeds were separated from the berries just before analysis at the laboratory and the soft parts of the berry (fruit flesh and peel) were used for all analysis. 2.2. Analysis of berry color, berry juice ratio, total soluble solids, pH and titratable acidity Skin color of sea buckthorn berries were recorded as L (brightness: 100, white; 0, black), a (+, red; , green) and b (+, yellow; , blue) values by using chromometer (Model CR 400, Konica Minolta Company, Japan). To determine the juice yield, a pressure extraction was used and calculated according to Tiitinen et al. (2005). Total soluble solid contents (TSS) of juice were determined at 22 8C as Brix by a digital refractometer (Kyoto Electronics Manufacturing Co. Ltd., Japan, Model RA-250HE) (Tiitinen et al., 2005). The pH measurements were made directly in berry juice using a digital pH meter (WTW Inolab Level 1, Germany) calibrated with pH 4 and 7 buffers (AOAC, 1984). Titratable acidity (%) was also measured directly in berry juice by a titrimetric method (AOAC, 1984). 2.3. Analysis of oil and fatty acids in berries Oil was extracted from the berries of sea buckthorn from different genotypes according to standard methods described by AACC (1983). Fatty acid composition was analyzed according to a previously published method (Anon., 2000) and fatty acids were separated by a gas chromatography (HP6890, Hewlett Packard, Palo Alto, CA, USA) using a fusedsilica capillary column (25 m  0.2 mm) with cross-linked 5% phenyl methyl silicone (Anon., 2000). 2.4. Analysis of ascorbic acid, total content of anthocyanins, antioxidant activity and total phenolic content The content of Vitamin C of sea buckthorn berries was determined in juice using the phenol indophenols dye method described by AOAC (1984). The content of total anthocyanin of the juice was determined by the pH differential method described by Wrolstad (1976). The antioxidant activity of the juice was determined according to the b-carotene bleaching method described by Kaur and Kapoor (2002) and compared butylated hydroxyanisole (BHA) and butylated hydroxytoluene (BHT) standards. The amount of total phenolics of sea buckthorn berries was determined in an ethanol extract by the Folin–Ciocalteau colorimetric method (Gulcin et al., 2002), and the results were expressed as mg gallic acid equivalents per g dry weight (mg GAE/g dw). 2.5. Analysis of mineral elements The mineral elements N, P, K, Ca, Mg, Na, Zn, Cu, Mn, Fe were determined according to James (1995).

S. Ercisli et al. / Scientia Horticulturae 115 (2007) 27–33

2.6. Statistical analysis The experiment consisted of a completely randomized design with four replications. Data were subjected to analysis of variance (ANOVA) and means were separated by Duncan multiple range test at P < 0.05 significant level. 3. Results and discussion 3.1. Berry color, berry juice yield, total soluble solids, pH and titratable acidity The present study revealed large significant (P < 0.05) difference among the investigated sea buckthorn genotypes for color, juice ratio, TSS and titratable acidity. The berry juice yield varied from 30.56 to 59.32%, with ESB-1 having the highest juice yield (Table 1). The fruit juice yield of sea buckthorn berries has previously been reported to vary between 60 and 80% (Sabir et al., 2005a). The cultivar has a low juice yield, which may be due to the origin of the plant material, geographical conditions or the applied agronomic practices. pH values of sea buckthorn juice varied from 2.63 (ESB-8) to 2.98 (ESB-1) which is in agreement with previously reported results for sea buckthorn in Finland (2.7–2.9 pH, Tiitinen et al., 2005). The titratable acidity was between 2.64% (ESB-1) and 4.54% (ESB-2) (Table 1). Tang and Tigerstedt (2001) reported a titratable acidity between 3.25 and 4.46% in sea buckthorn berries which is in accordance with our results. In the present study the TSS content varied between 10.15% (ESB-1) and 14.80% (ESB-5) (Table 1). This is also in agreement with previously reported data (7.4–12.6%, Tiitinen et al., 2005). Significant differences among genotypes (P < 0.05) were observed for lightness (L value), redness (a value) and yellowness (b value), and the results for the analysis of berry color varied from +33.50 (ESB-1) to +54.69 (ESB-7) for the L value, from 9.67 (ESB-9) to 30.94 (ESB-8) for the a value and from 37.44 (ESB-1) to 57.79 (ESB-10) for the b value (Table 1). According to results, ESB-7 had more brightness berries, ESB8 had more red berries and ESB-10 had more yellow berries. Tiitinen et al. (2005) reported L, a and b values in sea buckthorn

29

berries as 33.6–57.8, 4.0–18.5 and 22.8–45.7, respectively. These results support our findings. The range of estimates of quality characters of sea buckthorn berries thus seems to vary greatly among the studies cited, and among the regions considered by the researchers. This could be due to the specific geographical nature of the different areas and different agronomical practices. It is also well known that the plant genotype also strongly affect the physicochemical composition of sea buckthorn berries (Kawecki et al., 2004; Tiitinen et al., 2005, 2006). According to our results, ESB-1, provided the highest fruit juice yield and could be recommended for fruit juice production, whereas ESB-4, ESB-5 and ESB-6 may be considered for jam or jelly production due to higher TSS content. 3.2. Oil and fatty acid composition of sea buckthorn berries The pulp of ESB-5 contained the highest (3.4%) and ESB-1 contained the lowest (2.5%) amount of pulp oil. Pulp oil of sea buckthorn species naturally growing in Pakistan was found to be between 1.3 and 2.0% (Sabir et al., 2003), which is lower than in our study. Yellow and orange yellow berries have been reported to have higher level of oil than orange and orange-red berries (Daigativ et al., 1985). Most of our samples had yellow or yellow orange color (Table 1) which may be the reason for the high oil content. Ranjith et al. (2006) and Tiitinen et al. (2005) are reported pulp oil of fresh sea buckthorn berries between 1.49 and 3.60 and 0.70 and 3.60%, respectively, which is in accordance with our findings. The fatty acid analysis showed that the content of fatty acids varied among genotypes (P < 0.05; Table 2). The myristic acid was only detected in ESB-7 and ESB-8 genotypes and nervonic acid only detected in ESB-5 genotype. The dominant fatty acids in all genotypes were palmitoleic, palmitic, oleic and linoleic acids. The highest variation among the genotypes was observed in the proportion of palmitoleic acid (21.8–51.0%). ESB-1 genotype contained the highest proportion (51.0%) of this fatty acid in its berries. The variation in the next highest fatty acid, palmitic acid, was 19.9–35.8%. The presence of palmitoleic acid in berries of various sea buckthorn varieties and species has

Table 1 Color, berry juice ratio, pH, titratable acidity and total soluble solids (0Brix) contents of sea buckthorn genotypes Sample

ESB-1 ESB-2 ESB-3 ESB-4 ESB-5 ESB-6 ESB-7 ESB-8 ESB-9 ESB-10

Berry color L

a

b

33.50c 46.58b 48.60ab 53.75a 44.65ab 47.07ab 54.69a 53.10a 47.58ab 50.42ab

28.61a 16.80c 13.01cd 18.02bc 10.77cd 11.65cd 15.36c 30.94a 9.67d 22.02b

37.44b 48.38a 53.57a 55.63a 54.76a 52.14a 57.45a 54.28a 55.06a 57.79a

Berry juice ratio (%)

pH

Titratable acidity (%)

0

59.32a 52.63ab 53.32ab 50.10ab 47.94b 36.76bc 44.26bc 43.94bc 30.56c 31.37c

2.98 2.69 2.88 2.97 2.89 2.79 2.73 2.63 2.77 2.81

2.64c 4.54a 3.46b 3.31b 3.57b 3.75b 3.43b 4.41a 4.23a 3.88b

10.15b 11.80ab 13.00ab 14.35a 14.80a 14.15a 12.90ab 11.50ab 12.45ab 12.65ab

Values in the same column with different lower-case letters (a–d) are significantly different at *P < 0.05.

Brix

30

S. Ercisli et al. / Scientia Horticulturae 115 (2007) 27–33

Table 2 Fatty acid content (%) of sea buckthorn genotypes Fatty acids

ESB-1

ESB-2

ESB-3

ESB-4

ESB-5

ESB-6

ESB-7

ESB-8

ESB-9

ESB-10

X

Palmitic Palmitoleic Stearic Oleic Linoleic

19.9b 51.0a ND 14.9c 6.5ab

25.8ab 40.6b 1.4 19.4bc 4.6ab

30.5ab 33.0c 1.8 20.2bc 6.1ab

28.9ab 33.5c 1.5 26.5b 0.0b

25.4ab 34.9c 1.4 24.6ab 5.0a

24.9ab 41.3b 1.1 20.5bc 2.7ab

29.0ab 42.9b 1.0 14.3c 3.7ab

28.0ab 32.6c 1.3 22.7bc 3.8ab

33.1ab 21.8d ND 36.7a 1.8ab

35.8a 23.2d ND 29.1ab 5.4ab

28.13 35.48 0.95 22.89 3.96

Values in the same line with different lower-case letters (a–d) are significantly different at *P < 0.05. ND: Not detected.

previously been reported. Cakir (2004) investigated the fatty acid composition of one sea buckthorn genotype grown in Turkey and found that palmitoleic acid was the dominant fatty acid (47.8%) followed by palmitic (29.3%) and oleic acid (6.5%). This result is in agreement with our results. All our samples were characterized by high amounts of unsaturated fatty acids as compared to saturated analogues (Table 2). Our fatty acid results indicate a potential to develop palmitoleic acid rich varieties by plant selection and breeding. 3.3. Vitamin C, total content of anthocyanins, the antioxidant activity and the total phenolic content of berries The results for Vitamin C, total content of anthocyanins, the antioxidant activity and the total phenolic content of berries from different sea buckthorn genotypes are given in Figs. 1–4. The differences in Vitamin C content among different genotypes were statistically significant (P < 0.05; Fig. 1). The content of Vitamin C was only moderate, ranging from 19 (ESB-10) to 121 (ESB-8) mg/100 mL, respectively (Fig. 1). The genotype seemed to influence the extent of Vitamin C accumulation in the berries. According to earlier reports sea

buckthorn berries are high in Vitamin C, but that genetic background is the most important factor determining the Vitamin C content, and the degree of ripeness affects it more than other factors such as climatic conditions (Tang and Tigerstedt, 2001). Wild types of sea buckthorn have been reported to have lower Vitamin C than cultivated varieties (Kawecki et al., 2004). Previous studies have reported a typical variation of 2–500 mg/100 g of Vitamin C content in sea buckthorn berries (Gao et al., 2000; Sabir et al., 2005a; Tiitinen et al., 2006). In addition, the studies of Rousi and Aulin (1977) and Yao and Tigerstedt (1992) revealed a range of Vitamin C concentrations of 28–293 mg/100 g in berries from Finnish sea buckthorn bushes. Our Vitamin C results are thus in accordance with published literature. The total anthocyanin content of sea buckthorn berries ranged from 5 to 32 mg/L in berry juice and the differences among genotypes were found to be statistically significant (P < 0.05) (Fig. 2). The highest amount of anthocyanin was observed in ESB-8, while the lowest was in ESB-9. Relatively red berries, for example, ESB-8, were found to contain more anthocyanins than yellow (ESB-5) and light yellow (ESB-7) berries. The anthocyanin content of different sea buckthorn genotypes (H. rhamnoides) has previously been reported to be

Fig. 1. Vitamin C content of sea buckthorn genotypes. Values in the different lower-case letters are significantly different at *P < 0.05.

Fig. 2. Total anthocyanin content of sea buckthorn genotypes. Values in the different lower-case letters are significantly different at *P < 0.05.

S. Ercisli et al. / Scientia Horticulturae 115 (2007) 27–33

31

Fig. 3. Antioxidant activity of sea buckthorn genotypes and standards. Values in the different lower-case letters are significantly different at *P < 0.05.

between 0.5 and 25 mg/L (Sabir et al., 2005a) which is in accordance with our results. The antioxidant activity in berries of different sea buckthorn genotypes are shown in Fig. 3. A statistical significant difference (P < 0.05) was found among the samples, BHA and BHT. All samples revealed a very high antioxidant activity. The antioxidant activity reached nearly 100% for ESB-7 (93.55%) (which is similar to the standard BHT (93.26% at 200 mg/L)) and ESB-8 (92.56%) (Fig. 3). It has previously been reported that extracts of H. rhamnoides had strong antioxidant activity (Gao et al., 2000) which support our findings. The limitations of the present study of antioxidant activity are that it is based on only one analytic method. The amounts of total phenolics in different sea buckthorn genotypes are shown in Fig. 4. A great variation in terms of total phenolic content was observed among genotypes (21.31–55.38 mg GAE/g DW) and the differences were statistically significant (P < 0.05). ESB-4 had highest total phenolic content (55.38 mg GAE/g) followed by ESB-6 (54.75 mg GAE/g DW) and ESB-5 (50.06 mg GAE/g DW). There was no correlation (R = 0.688) between total phenolic content and antioxidant activity in the berry samples. Several studies have reported on the relationship between phenolic content and antioxidant activity. Some authors found a correlation between the phenolic content and the antioxidant activity, while others found no such relationship. Velioglu et al. (1998) reported a strong relationship between total phenolic content and antioxidant activity in certain plant products. Kahkonen et al. (1999) reported that no significant correlation could be found between the total phenolic content and the antioxidant activity of 92 plant extracts of the studied subgroups. In this study, no conclusive relationship between total phenolic content and antioxidant activity was found. For

example, ESB-7 had the highest level of antioxidant activity but had a medium level of total phenols. ESB-4 had one of the lower antioxidant activities but had the highest phenolic content. The results for total phenolics and antioxidant activity clearly suggest that sea buckthorn berries are one of the richest natural antioxidant sources among fruit species. The great difference among sea buckthorn genotypes in terms of total phenolics and antioxidant activity is supposed to be largely due to the genotype because all plants were grown in the same ecological condition. It has also previously been reported that plant genotype (Scalzo et al., 2005) affects total phenolic content in berry species. 3.4. Mineral elements of berries The mineral content of the different sea buckthorn genotypes are shown in Table 3. Statistical significant differences (P < 0.05) were observed among the sea buckthorn genotypes for the content of N, P, K, Ca and Zn (Table 3). These differences could be due to the natural content of elements in the soil, as well to contamination in both soil and air. The N, P, K and Ca values of sea buckthorn samples varied for N from 19,400 ppm (ESB-6) to 21,800 ppm (ESB-3); for P from 6000 ppm (ESB-1 and ESB-10) to 7600 ppm (ESB-3); for K from 6270 ppm (ESB-1) to 9240 ppm (ESB-7) and for Ca from 1232 ppm (ESB-1 and ESB-2) to 3696 ppm (ESB-5) (Table 3). Nitrogen is found to be the most abundant element in sea buckthorn berries in all samples followed by potassium, phosphorus, calcium and magnesium (Table 3). It has previously been reported that the potassium, calcium and magnesium content of sea buckthorn berry samples were between 6440 and 14,000, 270 and 3119 and 470 and 2222 ppm, respectively (Zeb, 2004) which is in agreement

Fig. 4. Total phenolic content of sea buckthorn genotypes. Values in the different lower-case letters are significantly different at *P < 0.05.

32

S. Ercisli et al. / Scientia Horticulturae 115 (2007) 27–33

Table 3 Mineral contents (ppm, dry weight basis) of sea buckthorn genotypes Minerals

ESB-1

ESB-2

ESB-3

ESB-4

ESB-5

ESB-6

ESB-7

ESB-8

ESB-9

ESB-10

N P K Ca Mg Na Zn Cu Mn Fe

20000b 6000b 6270e 1232d 1496 1395 38a 33 20 8

21000a 7500a 8030b 1232d 1479 1380 38ab 21 28 4

21800a 7600a 6600de 1408c 1428 1320 34ab 21 19 8

21500a 6800ab 6820d 3160a 1445 1410 32ab 30 28 8

21200a 7200ab 6490de 3696a 1462 1440 28ab 24 18 4

19400c 7400a 6490de 1760b 1428 1470 32ab 21 19 4

20200b 7000ab 9240a 1408c 1462 1380 32ab 18 21 4

21200a 7500a 7700b 1880b 1462 1365 30ab 24 19 4

21000a 6800ab 7260c 1936b 1530 1395 30ab 30 28 8

20400b 6600b 7700b 1880b 1462 1470 24b 18 20 10

Values in the same line with different lower-case letters (a–e) are significantly different at *P < 0.05.

with our results. Nitrogen and potassium was also found to be the most abundant element in sea buckthorn berries in some other studies (Chen, 1988; Tong et al., 1989; Zhang et al., 1989; Sabir et al., 2005b). The mineral composition of fruits depends, not only on the species or varieties, but also on the growing conditions such as soil and geographical condition (Chen, 1988). As a conclusion of this study, the present study reveals important and variable genotypic effects on physicochemical parameter of the berries. These differences may be very crucial for future plant breeding studies to obtain a plant which have a high amount of several important bioactive compounds in its berries. The great difference among genotypes in terms of physicochemical profile also show their potential use for further breeding studies. Acknowledgement The authors want to thank Kimmo Rumpunen, Swedish University of Agricultural Sciences, Balsgard, for valuable comments on the manuscript. References AACC, 1983. Approved Methods of American Association of Cereal Chemists. The American Association of Cereal Chemist Inc., St. Paul, Minnesota, USA. Anon., 2000. Sherlock Microbial Identification System. Version 4 MIS Operating Manual, Newark, DE, USA. AOAC, 1984. Officials Methods of Analysis, 14th ed. Association of Official Analytical Chemist, Arlington, VA, USA. Baytop, T., 1999. Therapy with Medicinal Plants in Turkey (Past and Present). Nobel Press, Istanbul. Cakir, A., 2004. Essential oil and fatty acid composition of the fruits of Hippophae rhamnoides L. (sea buckthorn) and Myrtus communis L. from Turkey. Biochem. Syst. Ecol. 32 (9), 809–816. Chen, T., 1988. Studies of the biochemical composition of Hippophae and its quality assessment in Gansu Province. Hippophae 1, 19–26. Daigativ, D.D., Muratchaeva, P.M., Magomedmirzaev, M.M., 1985. Correlation of some fruit characteristics with lipid and tocopherol content in Hippophae rhamnoides L. Rastit. Resur. (Russian) 21, 283–289. Gao, X., Ohlander, M., Jeppsson, N., Bjork, L., Trajkovski, V., 2000. Changes in antioxidant effects and their relationship to phytonutrients in fruits of sea buckthorn (Hippophae rhamnoides L.) during maturation. J. Agric. Food Chem. 48, 1485–1490.

Gulcin, I., Oktay, M., Kufrevioglu, I., Aslan, A., 2002. Determination of antioxidant activity of lichen Cetraria islandica (L.) Ach. J. Ethnopharmacol. 79, 325–329. Guliyeva, V.B., Gul, M., Yildirim, A., 2004. Hippophae rhamnoides L.: chromatographic methods to determine chemical composition, use in traditional medicine and pharmacological effects. J. Chromatogr. B 812, 291–307. James, G.S., 1995. Analytical Chemistry of Foods. Blackie Academic and Professional, London, pp. 117–120. Kahkonen, M.P., Hopia, A.I., Vuorela, H.J., Rauha, J.P., Pihlaja, K., Kujala, T.S., Heinonen, M., 1999. Antioxidant activity of plant extracts containing phenolic compounds. J. Agric. Food Chem. 47, 3954–3962. Kaur, C., Kapoor, H.C., 2002. Anti-oxidant activity and total phenolic content of some Asian vegetables. Int. J. Food Sci. Technol. 37, 153–161. Kawecki, Z., Szalkiewicz, M., Bieniek, A., 2004. The common sea buckthorn— a valuable fruit. J. Fruit Ornamental Plant Res. 12, 183–193. Lu, R., 1992. Seabuckthorn: A Multipurpose Plant Species for Fragile Mountains. ICIMOD Publication Unit, Katmandu, Nepal. Meyskens, F.L., Szabo, E., 2005. Diet and cancer: the disconnect between epidemiology and randomized clinical trials. Cancer Epidemiol. Biomarkers Prev. 14, 1366–1369. Nakamura, Y., Watanabe, S., Miyake, N., Kohno, H., Osawa, T., 2003. Dihydrochalcones: evaluation as novel radical scavenging antioxidants. J. Agric. Food Chem. 51, 3309–3312. Ranjith, A., Kumar, K.S., Venugopalan, V.V., Arumughan, C., Sawhney, R.C., Singh, V., 2006. Fatty acids, tocols, and carotenoids in pulp oil of three sea buckthorn species (H. rhamnoides, H. salicifolia, and H. tibetana) grown in the Indian Himalayas. JAOCS 88, 359–364. Robards, K., Prenzler, P.D., Tucker, G., Swatsitang, P., Glover, W., 1999. Phenolic compounds and their role in oxidative processes in fruits. Food Chem. 4, 401–436. Rousi, A., Aulin, H., 1977. Ascorbic acid content in relation to ripeness in fruits of six Hippopha rhamnoides clones from Pyharanta, SW Finland. Ann. Agric. Fenn. 16, 80–87. Sabir, S.M., Ahmed, S.D., Lodhi, N., 2003. Morphological and biochemical variation in Hippophae rhammnoides ssp. turketanica, a multipurpose plant for fragile mountains of Pakistan. S. Afr. J. Bot. 69, 587–592. Sabir, S.M., Maqsood, H., Ahmed, S.D., Shah, A.H., Khan, M.Q., 2005a. Chemical and nutritional constituents of sea buckthorn (Hippophae rhamnoides ssp. turkestanica) berries from pakistan. Ital. J. Food Sci. 17, 455–462. Sabir, S.M., Maqsood, H., Hayat, I., Khan, M.Q., Khalid, A., 2005b. Elemental and nutritional analysis of sea buckthorn (Hippophae rhamnoides ssp. turketanica) berries of Pakistani origin. J. Med. Food 8, 518–522. Scalzo, J., Politi, A., Pellegrini, N., Mezzetti, B., Battino, M., 2005. Plant genotype affects total antioxidant capacity and phenolic contents in fruit. Nutrition 21, 207–213. Tang, X., Tigerstedt, P.M.A., 2001. Variation of physical and chemical characters within an elite sea buckthorn (Hippophae rhamnoides L.) breeding population. Sci. Hort. 88, 203–214. Tiitinen, K.M., Hakala, M.A., Kallio, H.P., 2005. Quality components of sea buckthorn (Hippophae rhamnoides) varieties. J. Agric. Food Chem. 53, 1692–1699.

S. Ercisli et al. / Scientia Horticulturae 115 (2007) 27–33 Tiitinen, K.M., Yang, B., Haraldsson, G.G., Jonsdottir, S., Kallio, H.P., 2006. Fast analysis of sugars, fruit acids, and Vitamin C in sea buckthorn (Hippophae rhamnoides) varieties. J. Agric. Food Chem. 54, 2508– 2513. Tong, J., Zhang, C., Zhao, Z., Yang, Y., Tian, K., 1989. The determination of physical–chemical constants and sixteen mineral elements in sea buckthorn raw juice. In: International Symposium Sea Buckthorn (H. rhamnoides L.) p. 132. Velioglu, Y.S., Mazza, G., Gao, L., Oomah, B.D., 1998. Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. J. Agric. Food Chem. 46, 4113–4117.

33

Wrolstad, R.E., 1976. Color and pigment analyses in fruit products. Oregon St. Univ. Agric. Exp. Stn. Bull. 624, 1–13. Yao, Y., Tigerstedt, P., 1992. Variation of Vitamin C concentration and character correlation between and within natural sea buckthorn (Hippophae rhamnoides L.) populations. Acta Agric. Scand. 42, 12–17. Zeb, A., 2004. Chemical and nutritional constituents of sea buckthorn juice. Pak. J. Nutr. 3, 99–106. Zhang, W., Yan, J., Duo, J., Ren, B., Guo, J., 1989. Preliminary study of biochemical constitutes of berry of sea buckthorn growing in Shanxi Province and their changing trend. In: International Symposium Sea Buckthorn (H. rhamnoides L.) p. 96.