HippophaÃ« rhamnoides L. - ACS Publications - American Chemical

Article Cite This: J. Agric. Food Chem. 2017, 65, 9871-9879

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Role of Flavonols and Proanthocyanidins in the Sensory Quality of Sea Buckthorn (Hippophaë rhamnoides L.) Berries Xueying Ma,† Wei Yang,† Oskar Laaksonen,† Merja Nylander,† Heikki Kallio,† and Baoru Yang*,†,‡ †

Food Chemistry and Food Development, Department of Biochemistry, University of Turku, FI-20014 Turku, Finland Department of Food Science and Engineering, Jinan University, 510632 Guangzhou, China

‡

S Supporting Information *

ABSTRACT: Sensory profile, flavonols, proanthocyanidins, sugars, and organic acids were investigated in purees of six sea buckthorn (Hippophaë rhamnoides) cultivars. The sensory profiles of the purees were dominated by intense sourness followed by astringency and bitterness due to the high content of malic acid. Malic acid and isorhamnetin glycosides, especially isorhamnetin3-O-sophoroside-7-O-rhamnoside, had close association with the astringent attributes in the different purees, whereas some of the known astringent compounds such as proanthocyanidin dimers and trimers or quercetin glycosides, had less impact. Moreover, the ratios between contents of acids and phenolic compounds were more important predictors of bitterness than the individual variables alone. Astringency and bitterness are important sensory factors for the consumer acceptance of sea buckthorn products. The current study provides new knowledge on the correlations between sensory properties and composition and supports industrial utilization of the sea buckthorn berries. KEYWORDS: astringency, bitterness, flavonol glycosides, Hippophaë rhamnoides, proanthocyanidins, sea buckthorn, sensory profile

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their use as foods.6 The bitterness of the SB juices correlates with the content of ethyl β-D-glucopyranoside (EG).23 The taste and astringent properties of nonvolatile phenolic compounds have been studied in some berries. The content of FGs is associated with astringency, and the content of PAs is positively associated with the mouth-drying and puckering astringent characteristics.20,24,25 The composition and quantity of phenolic compounds has attracted much attention in the SB berry, but the contribution of these compounds to the sensory quality of the SB berry is not yet well described. The juice fractions of the berries are commonly utilized in food industry, whereas the skin and seeds are side products often left unused. Most studies have typically focused on the chemical composition of the whole fruit, although some studies demonstrated high concentration of a variety of astringent and bitter phenolic compounds primarily in the skin fractions of berries.24,25 Furthermore, the profiles of phenolic compounds differ among fractions (seed, skin, and pulp) of berries.26 Sea buckthorn puree has become increasingly popular as a consumer product and an ingredient for various foods. Sea buckthorn puree is prepared with a process involving removal of seeds, retaining most soft parts (fruit pulp and peel) of the berries. The aim of this study was to investigate the role of phenolic compounds in the sensory quality of berry puree by studying the sensory profiles of six SB cultivars. The cultivars chosen were commonly cultivated commercial cultivars belonging to two subspecies (ssp. rhamnoides and ssp. mongolica) of sea buckthorn. The berry samples were collected from growth sites

INTRODUCTION Phenolic compounds such as flavonoids and phenolic acids are secondary metabolites commonly found in plants and plantbased foods. Currently, edible plants rich in phenolic compounds are receiving considerable attention for their health benefits related to cardiovascular diseases, metabolic syndrome, neurodegenerative disorders, and certain kinds of cancer.1,2 In particular, due to presumed effects on the gut microbiota, polymeric phenolic compounds like proanthocyanidins (PAs) are gaining credence as bioactive molecular species.3 Moreover, many phenolic compounds, especially flavonol glycosides (FGs) and PAs in foods, contribute to astringency and bitterness,4,5 which are often regarded as negative sensory characteristics by consumers.6,7 Sea buckthorn (Hippophaë rhamnoides, SB) berries are a rich source of flavonols8−10 and also contain notable amounts of procyanidins.11,12 The content of the phenolic compounds in the berry varies with origin, weather condition, growth location, latitude, and harvest date.8−10,12−15 FGs have been found to induce a silky, mouth-drying, and mouth-coating astringent sensation even at very low concentrations, and they are not generally perceived as bitter.16,17 However, flavonol aglycons (FAs) may activate bitter taste receptors.18 PAs are well-known astringent and bitter components in plant-based foods and beverages. Although PAs are found at lower contents than flavonol glycosides in SB berries, they may have an essential role in the astringent and bitter sensation due to their relatively low threshold.16,19,20 Sensory quality is an important factor influencing the food choice of consumers. In general, the contents of sugars and acids as well as the sugar/acid ratio play a crucial role in determining the flavor and consumer acceptance of berries and berry products.21,22 Bitterness and astringent properties are often considered as negative features in berries and may limit © 2017 American Chemical Society

Received: Revised: Accepted: Published: 9871

September 6, 2017 October 13, 2017 October 16, 2017 October 16, 2017 DOI: 10.1021/acs.jafc.7b04156 J. Agric. Food Chem. 2017, 65, 9871−9879

Article

Journal of Agricultural and Food Chemistry

Identification was based on UV−vis spectra, retention times, and the results described earlier, and the compounds were quantified with an external standard method as previously described.8,10 Quantitative analysis of flavonol glycosides was carried out using quercetin-3-Orutinoside, quercetin-3-O-glucoside, isorhamnetin-3-O-glucoside, and isorhamnetin-3-O-rutinoside as the external standards. Quercetin-3-Osophoroside-7-O-rhamnoside was quantified as quercetin-3-O-rutinoside equivalents. Isorhamnetin-glucoside was quantified as isorhamnetin-3-O-glucoside; isorhamnetin-rutinoside was quantified as isorhamnetin-3-O-rutinoside, and other isorhamnetin glycosides were quantified as equivalents of isorhamnetin-3-O-rutinoside. Standard solutions of quercetin-3-O-rutinoside, quercetin-3-O-glucoside, isorhamnetin-3-O-glucoside, and isorhamnetin-3-O-rutinoside in methanol were in the concentration range of 0.007−1.2 mg/mL. The correlation coefficients (R2) of the standard curves varied from 0.9971 to 0.9997. Qualitative and Quantitative Analysis of Proanthocyanidins. Extraction and purification of PAs from the sea buckthorn puree were carried out according to our previous methods.12 The quantitative analysis was conducted using a Waters Acquity Ultra High Performance LC system (Waters Corp., Milford, MA) coupled with a Waters Quattro Premier Tandem Quadrupole mass spectrometer (Waters Corp., Milford, MA). A Phenomenex Luna HILIC 200A column (3 μm, 150 × 3.00 mm, Torrance, CA) was employed to separate PAs. The gradient program of LC and ESI-MS conditions were the same as those described earlier.12 Quantitative analysis of PA oligomers (dimers, trimers, and tetramers) was carried out using HILIC-ESI in single ion recording (SIR) and procyanidin B2 as an external standard.27 The peak areas of PA oligomers in SIR mode were corrected by ionization efficiency, which operated by epicatechin in a proper molar concentration. The contents of oligomeric PAs were determined against a standard curve of procyanidin B2 constructed within a concentration range of 0.01 to 10 mg/100 mL.12 The contents of total PAs were determined by the Brunswick Laboratories 4-dimethylaminocinnamaldehyde (BL-DMAC) assay as procyanidin B2 equivalent.12 The contents of total PAs were assessed by a colorimetric method using the calibration curve of procyanidin B2 (1−20 mg/mL) constructed by plotting the OD values against the concentration. Quantitative Analysis of Sugars and Organic Acids. Individual sugars and organic acids were analyzed by gas chromatography (GC) as trimethylsilyl (TMS) derivatives using the method described previously with some modifications.28 About 5 g of puree was centrifuged at 4360g for 10 min, and the juice was separated. The internal standards sorbitol and tartaric acid were used for quantification. Correction factors determined with reference compounds were used to quantify individual compounds of sugars and acids. Ethyl β-D-glucopyranoside was quantified as glucose. The column and instrument conditions were the same as those described previously.23 The analytes were identified by coinjection of the reference compounds and quantified by an internal standard method.28 Sensory Analysis. Sensory characteristics of the purees were evaluated using a generic descriptive analysis. Twelve panelists were trained according to the ISO 8586-1 standard to evaluate the samples of different cultivars. The training sessions and test sessions were completed in one month. The selection of the descriptors was based on investigations of Tiitinen et al.21 and Laaksonen et al.29 Eight sensory attributes were chosen for evaluations (Supplementary Table 1). The two astringent references were perceived to be notably different at the concentrations used in Supplementary Table 1.22 The panelists were trained to focus on the subqualities instead of the whole astringent sensation. The intensities of the attributes were rated on a continuous graphical scale, from 0 (none) to 10 (very strong) with the help of anchored reference samples (Supplementary Table 1). The sea buckthorn purees were kept at room temperature for 20−30 min before sensory analysis. The samples were mixed and divided into aliquots of 2 mL in 50 mL transparent plastic beakers covered with lids that were randomly coded with three-digit numbers. The samples were evaluated in triplicate in separate sessions as blind coded and in randomized order. The data were collected using Compusense-f ive software (version 5.6, Compusense, Guelph, Canada).

in Finland and Estonia. The ultimate goal of the study is to produce new scientific knowledge on sensory properties of sea buckthorn, providing guidance on its breeding, cultivation, and utilization.

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MATERIALS AND METHODS

Puree Samples. Berries of sea buckthorn cultivars “Terhi” and “Tytti” of Hippophaë rhamnoides ssp. rhamnoides were collected in Turku, Finland, in August 2015. The berries of SB cultivars “Hergo” and “Leikora” of H. r. ssp. rhamnoides and “Trofimovskaya” and “Avgustinka” of H. r. ssp. mongolica were collected in Rö hu experimental station of Estonia in September 2015. All of the berries were picked when optimally ripe as defined by experienced horticulturists. Berries were frozen loosely immediately after picking and stored at −20 °C for analysis. Batches of about 200 g of sea buckthorn berries were taken from a 1 kg berry pool. The berry batches were gently thawed in a microwave oven (Whirlpool MW 201, Fonthill Industrial Estate, Dublin, Ireland) with 90 W for 2 × 30 s, and then the seeds were removed by hand. The berries without seeds were homogenized to purees with a Bamix M133 mixer (Bamix, Mettlen TG, Switzerland). The puree batches were prepared on the day before each of the three replicate sensory evaluation sessions. The purees were divided into two parts: one part was stored at 4 °C overnight for sensory evaluations, and the other at −20 °C for chemical analysis. The chemical analysis of puree samples was finished within one month. Chemicals and Reagents. Dichloromethane and formic acid (both HPLC grade) were purchased from J. T. Baker (Deventer, Holland), and methanol (HPLC grade), tetrahydrofuran (HPLC grade), trifluoroacetic acid (HPLC grade), acetone (HPLC grade), and acetonitrile (HPLC and MS grade) were from VWR International Oy (Espoo, Finland). Reference compounds, D-fructose, quinic acid, and ascorbic acid were purchased from Sigma Chemical Co. (St. Louis, MO, United States). D-glucose and the internal standard D-sorbitol (for sugars) were purchased from Fluka (Buchs, Switzerland). Malic acid and the internal standard tartaric acid (for acids) were purchased from Merck (Darmstedt, Germany). Citric acid was purchased from J. T. Baker (Deventer, Holland). L-quebrachitol (1-L-2-O-methyl-chiroinositol) was purchased from Alexis Corporation (Läufelfingen, Switzerland). Reference compounds (≥99%) procyanidin B2, quercetin-3-O-rutinoside, quercetin-3-O-glucoside, isorhamnetin-3-O-glucoside, and isorhamnetin-3-O-rutinoside were purchased from Extrasynthese (Genay, France). Reference compounds isorhamnetin-3-Oglucoside-7-O-rhamnoside, isorhamnetin-3-O-sophoroside-7-O-rhamnoside, and quercetin-3-O-sophoroside-7-O-rhamnoside isolated from sea buckthorn berries were provided by Professor Zhang Hao and Professor Lothar W. Kroh.8 Water was purified with PURELAB Ultra Scientific system (ELGA, UK). Quantitative Analysis of Flavonol Glycosides. Extraction of FGs from the sea buckthorn purees was carried out according to our previous method.8 High-performance liquid chromatography-diodearray detection (HPLC-DAD) analysis was performed according to the method applied earlier by our group with modifications.8 The HPLC-DAD instrument consisted of a Shimadzu (Shimadzu Corporation, Kyoto, Japan) SIL-30AC auto sampler, a sample cooler, two LC-30AD pumps, a CTO-20AC column oven, an SPD-M20A diode array detector, and a CBM-20A central unit. The system was operated using LabSolutions Workstation software. A Phenomenex Aeris peptide XB-C18 (3.6 μm, 150 × 4.60 mm) column combined with a Phenomenex Security Guard Cartridge Kit (Torrance, CA) was used at an oven temperature of 40 °C for analysis. The mobile phase consisted of a binary gradient elution system. Solvent A was a mixture of water, tetrahydrofuran, and trifluoroacetic acid (98:2:0.1, v/v/v), and solvent B was acetonitrile. The elution gradient program was as follows: 0−3 min, 15% B; 3−10 min, 15−25% B; 10−15 min, 25−60% B; 15−20 min, 60−15% B; 20−25 min, 15% B. The flow rate of the mobile phase was 1 mL/min, and the injection volume was 10 μL. The peaks were monitored at 360 nm with a DAD. The contents of FGs were expressed as mg/100 g fresh weight (FW). 9872

DOI: 10.1021/acs.jafc.7b04156 J. Agric. Food Chem. 2017, 65, 9871−9879

Article

Journal of Agricultural and Food Chemistry Statistical Analysis. All samples were prepared and analyzed in triplicate. Statistical analyses were carried out with SPSS 22.0 (SPSS, Inc., Chicago, IL). One-way ANOVA together with Tukey’s HSD and the Tamhane test were used for comparing chemical variances of different cultivars. Three-way ANOVA was used for sensory results with samples as fixed factors and sessions and panelists as random factors. Differences reaching a minimal confidence level of 95% were considered as being statistically significant. The partial least-squares (PLS) regression was used to investigate relationships between the compositional variables (X-data, n = 40), some ratios between compounds (Supplementary Table 2, X-data, n = 37), and the averaged sensory attributes (Y-data, n = 8) in the 6 sea buckthorn purees. Full cross validation was used to determine the number of validated factors, and unit variance scaling was used for the data in the regression models. Multivariate models were created with Unscrambler 10.3 (Camo Process AS, Oslo, Norway).

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(22.3−38.0% of total FGs) were the two major FGs in all the samples (Table 1). Statistically significant differences were found in the content of most FGs among the purees prepared from berries of different cultivars (Table 1). “Leikora” had higher content of isorhamnetin-glucoside-rhamnoside, isorhamnetin-3-O-glucoside-7-O-rhamnoside, isorhamnetin-3-O-rutinoside, and total FGs compared with that found in other cultivars (p < 0.05). In contrast, the lowest content of these compounds existed in the cultivar “Avgustinka” compared with that in other cultivars (p < 0.05). The total content of FGs in “Leikora” was nearly 3-fold higher compared with that in “Avgustinka”. The cultivar “Terhi” contained the highest ratio of Is/Qu, and “Trofimovskaya” contained the lowest (p < 0.05). The isolated proanthocyanidin fractions were analyzed by HILIC-ESI-MS in negative ion mode (m/z 500 to 3000). The total ion spectra showed similar oligomer profiles in all six cultivars. Only single-charged molecular ions of PAs with degrees of polymerization (DP) from 2 to 4 (PA dimers, trimers, and tetramers) were detected. No multicharged molecular ions of PAs were found. All compounds represented the B-type PAs. Figure 1B shows the [M − H]− ions of PA dimers (m/z 593.7 for Dim-2 and m/z 609.6 for Dim-3), PA trimers (m/z 866.0 for Tri-1, m/z 881.6 for Tri-2, m/z 897.8 for Tri-3, and m/z 913.7 for Tri-4), and PA tetramers (m/z 1155.2 for Tet-1, m/z 1170.3 for Tet-2, m/z 1186.5 for Tet-3, m/z 1201.4 for Tet-4, and m/z 1217.3 for Tet-5). As shown in our previous study,27 (epi)-catechin and (epi)-gallocatechin were the two monomer units of PAs in sea buckthorn berries. These flavan-3-ol monomer units linked via C4−C8 and/or

RESULTS AND DISCUSSION

Phenolic Profiles. The results of flavonol glycosides in the puree samples were in accordance with our earlier reports of whole berries.8,10 Ten major FGs identified previously are marked in Figure 1A, of which the sum was taken as total FGs.8 Total content of FGs ranged from 59.2 to 169.1 mg/100 g of FW in this study (Table 1). Glycosides of isorhamnetin represented the highest percentage and diversity among FGs in all the samples analyzed, as reported earlier.8,10 Isorhamnetin (Is) and quercetin (Qu) were the predominant aglycon moieties in the flavonol glycosides among the samples (85.4−95.5 and 4.5−14.6%, respectively), and isorhamnetin-3-O-rutinoside (20.3−39.9% of total FGs) and isorhamnetin-3-O-glucoside-7-O-rhamnoside

Figure 1. Example chromatograms of the LC analyses of major phenolics in sea buckthorn puree (cultivar “Leikora”). (A) HPLC-DAD chromatogram (at 360 nm) of the flavonols. (B) Total ion spectrum of PAs from 3.6 to 17.5 min analyzed by HILIC-ESI-MS. Is, isorhamnetin; Qu, quercetin; G, glucoside; Rh, rhamnoside; R, rutinoside; S, sophoroside; PAs, proanthocyanidins. 9873


Article

± ± ± ± ± ± 98.5 93.6 119.9 169.1 92.0 59.2 0.5 0.1a 1.3d 0.4e 0.4c 0.1a

± ± ± ± ± ± 11.6 9.0 17.1 25.7 14.7 10.1 0.2 0.0c 0.0c 0.1d 0.0b 0.0a

± ± ± ± ± ± 0.9 0.3d 1.0e 1.0f 0.4c 0.3a 0.1 0.0c 0.0a 0.1f 0.0d 0.0b

19.7 30.9 47.9 50.1 24.3 12.0

± ± ± ± ± ±

b

± ± ± ± ± ± 0.4 0.2c 0.5d 0.2b 0.1a 0.1a 0.0 0.0a 0.0a 0.0c 0.1b 0.0a

± ± ± ± ± ± 0.9 0.7 0.7 1.0 0.8 0.7

b

Tytti Terhi Hergo Leikora Trofimovskaya Avgustinka

9.5 7.4 9.4 5.8 3.0 3.4

d

9.2 4.1 4.9 10.7 3.4 2.3 ± ± ± ± ± ±

e

0.4 0c 0.2d 0.2f 0.0b 0.1a

34.7 35.6 29.0 55.2 29.8 13.2

± ± ± ± ± ±

c

1.8 0.7c 1.1b 1.2d 0.5b 0.1a

3.9 2.0 4.5 6.9 6.9 2.4

± ± ± ± ± ±

c

0.2 0.1a 0.1d 0.1e 0.2e 0.0b

2.2 1.5 2.9 4.4 5.3 3.0

± ± ± ± ± ±

b

0.1 0.0a 0.1c 0.3d 0.4e 0.1c

2.5 1.5 0.8 5.6 1.8 1.2

± ± ± ± ± ±

e

Is-3-R Is-R Qu-3-G Qu-3-R Is-3-G-7-Rh Is-G-Rh Is-3-S-7-Rh Qu-3-S-7-Rh cultivars

Table 1. Flavonol Glycosides in Sea Buckthorn Purees (mg/100 g FW)a

C4−C6 carbon−carbon bonds form B-type PAs. Within each degree of polymerization, the type of subunit determines the molecular weight of PAs. The [M − H]− ions were detected with 16 amu differences among PA oligomers with the same DP value due to variation in the number of (epi)-catechin and (epi)-gallocatechin as subunits of PAs. Compared with our previous study, some differences in the profiles between whole SB berries (with seeds) and SB puree (without seeds) were detected. PAs of DP from 5 to 11 and a PA dimer with a deprotonated molecular ion [M − H]− at m/z 577 (Dim-1) was detected only in whole berries.12,27 Moreover, the deprotonated molecular ions of PA trimers and tetramers did not appear in significant amounts in SB purees. We speculate that the majority of PAs, especially PAs with DP > 4 in sea buckthorn, are mainly present in the seeds. As reported by Downey et al, the subunit composition of PAs was different in the seeds and skin of grapes.30 Furthermore, the genes encoding leucoanthocyanidin reductase, which is essential for the biosynthesis of flavan-3-ols as monomeric units of PA polymers, had different patterns of expression in the skin and seeds of grapes.31 This indicates that different fractions of berries/fruits may have different profiles of PAs. The contents of PAs listed in Table 2 are the average values of triplicate samples. The content of PA dimers, trimers, and tetramers was in the range of 0.14−3.50, 0.22−1.97, and 0.12−1.71 mg/100 g, respectively, accounting for only a small proportion (0.30−14.4%) of the total PAs (23.0−47.4 mg/100 g) in the puree samples studied (Table 2). The differences in contents between PA oligomers and total PAs were due to the different measurement methods. The LC-MS method was only for PA oligomers (dimers, trimers, and tetramers) with specific molecular masses. However, PA monomers, oligomers, and polymers were all taken into account in the content of total PAs based on DMAC method. The cultivar “Trofimovskaya” was the richest source of dimers, trimers, and tetramers, but it contained fewer total PAs compared with the rest of the cultivars (p < 0.05, Table 2). “Terhi” had the lowest content of dimers, whereas the fewest trimers and tetramers were found in “Avgustinka” (p < 0.05, Table 2). The highest and the lowest total content of PAs were found in “Hergo” (70.2 mg/100 g of FW) and “Avgustinka” (23.0 mg/100 g of FW), respectively. Sugars and Organic Acids. The contents of sugars and organic acids in sea buckthorn purees are shown in Table 3. Results of the present study revealed clear and significant differences in the content of sugars and acids in all cultivars. Fructose and glucose were the two major sugars, and malic and quinic acids were the major organic acids in the SB purees studied. Glucose was the most abundant sugar in all the cultivars except “Hergo”, contents varied from 0.2 to 4.8 g/100 g (FW) among the cultivars. Among all the cultivars, malic acid (53.8−74.1% of total acid) appeared as the most abundant acid, and the contents varied from 1.6 to 4.0 g/100 g (FW). The highest content of total sugars and the lowest content of total acids were found in “Trofimovskaya” with the highest ratio of sugars to acids (3.0), whereas this ratio was only 0.1 in “Hergo”. Sensory Profiles. Overall, all the samples were perceived as notably sour, bitter, and puckering astringent as well as sharp. Statistically significant differences among the puree samples (three-way ANOVA together with Tukey’s post hoc test; p < 0.05) were detected in six out of eight evaluated flavor descriptors (Table 4). The scores of four attributes correlated with total intensity of flavor (Table 4), indicating their important

a Means ± standard deviation of three replicates. The letters a−f mark the significant statistical differences based on one-way ANOVA with Tukey’s HSD (p < 0.05). FGs, flavonol glycosides; FAs, flavonol aglycons; G, glucoside; Is, isorhamnetin; Qu, quercetin; Rh, rhamnoside; R, rutinoside; S, sophoroside. bRatio between total isorhamnetin aglycon and total quercetin aglycon in all FGs.

2.3b 0.8b 1.9c 1.2d 0.9b 0.3a ± ± ± ± ± ± 51.6 49.3 63.2 90.1 49.5 26.9 4.5 1.8b 3.5c 2.3d 1.5b 0.4a

12.9 21.1 13.3 12.6 5.9 6.9

± ± ± ± ± ±

0.2 0.4e 0.3d 0.4c 0.2a 0.0b

cd

4.4 2.5 2.6 3.7 1.9 1.4

Is-G

e

Is-3-G

b

total FGs

b

Is/Qu ratiob

total FAs


9874


Tet-1

Tet-2

Tet-3

Tet-4

Tet-5

dimers

trimers

tetramers

total PAs

0.00 ± 0.0a

0.15 ± 0.06a 0.01 ± 0.0a

0.04 ± 0.0a 0.08 ± 0.01a 0.09 ± 0.01a 0.01 ± 0.0a 0.01 ± 0.0a

0.02 ± 0.0a 0.04 ± 0.0a 0.04 ± 0.01a 0.16 ± 0.06a 0.22 ± 0.02a 0.12 ± 0.01a 23.0 ± 2.4a

9875

2.8 2.7 2.7 2.8 3.2 3.0


7.5 7.4 7.7 6.9 9.6 8.5

°Brix

0.1 0.1 0.1 0.1 2.4 0.3

± ± ± ± ± ± a

0.0 0.0a 0.0a 0.0a 0.4b 0.0a

fructose 0.0 0.0a 0.0a 0.0a 0.8c 0.1b

0.1 0.2 0.2 0.3 0.2 0.1

0.0 0.0b 0.0ab 0.0c 0.0b 0.0a

± ± ± ± ± ±

0.7 0.6 0.2 0.4 4.8 3.2

ab

± ± ± ± ± ± a

L-quebrachitol

glucose 0.2 0.0 0.3 0.1 0.2 0.7

± ± ± ± ± ± a

0.0 0.0a 0.0b 0.0a 0.0a 0.1c

EG 1.0 0.8 0.5 0.8 7.4 3.6

± ± ± ± ± ± 0.0 0.0a 0.0a 0.0a 1.2c 0.1b

a

total sugarsb 4.0 3.6 2.8 3.1 1.6 1.8

± ± ± ± ± ±

0.2 0.1c 0.1b 0.2b 0.3a 0.0a

d

malic acid

0.08 0.04 0.02 0.04 0.03 0.02

± ± ± ± ± ±

b

0.0 0.0a 0.0a 0.0a 0.0a 0.0a

citric acid

1.1 1.7 2.2 1.0 0.7 1.2

± ± ± ± ± ±

0.0 0.0d 0.1e 0.1b 0.1a 0.1c

bc

quinic acid

0.2 0.1 0.1 0.3 0.1 0.2

± ± ± ± ± ±

0.0 0.0bc 0.0a 0.0d 0.0b 0.0c

c

ascorbic acid

5.4 5.4 5.2 4.3 2.4 3.2

± ± ± ± ± ±

0.3 0.2d 0.2d 0.2c 0.4a 0.1b

d

total acids

0.2 0.2 0.1 0.2 3.0 1.2

± ± ± ± ± ±

0.0b 0.0ab 0.0a 0.0b 0.0d 0.0c

sugar/acid ratio

a Means and standard deviations of three replicates, except for one replicate in pH and °Brix. Significant differences between sensory samples in each variable are based on one-way ANOVA with Tukey’s HSD. Test (p < 0.05) are marked with a−e. bIncludes fructose, glucose, and L-quebrachitol but not ethyl β-D-glucopyranoside (EG).

pH

cultivars

Table 3. pH, °Brix, Sugars, and Organic Acids in Sea Buckthorn Purees (g/100 g FW)a

a Means ± standard deviation of three replicates; significant differences between cultivars based on one-way ANOVA with Tukey’s HSD (p < 0.05) are marked as a−d. Dimers are sums of Dim-2 and Dim-3; trimers are sums of Tri-1, Tri-2, Tri-3, and Tri-4, and tetramers are sums of Tet-1, Tet-2, Tet-3, Tet-4, and Tet-5. Total PAs were determined by DMAC.

Avgustinka

Trofimovskaya 0.02 ± 0.0bc 3.48 ± 0.83c 0.23 ± 0.06c 0.48 ± 0.09c 0.69 ± 0.12c 0.58 ± 0.1b 0.30 ± 0.06b 0.40 ± 0.08d 0.35 ± 0.07c 0.36 ± 0.06b 0.30 ± 0.04b 3.50 ± 0.84c 1.97 ± 0.36c 1.71 ± 0.31c 24.3 ± 3.4a

0.02 ± 0.0bc 1.17 ± 0.29b 0.09 ± 0.01b 0.20 ± 0.02b 0.39 ± 0.03b 0.43 ± 0.04b 0.08 ± 0.01a 0.16 ± 0.02c 0.19 ± 0.03b 0.28 ± 0.04b 0.28 ± 0.01b 1.19 ± 0.29b 1.11 ± 0.34b 0.99 ± 0.09b 45.9 ± 7.5b

Tri-4

Leikora

Tri-3

0.04 ± 0.02cd 0.73 ± 0.15ab 0.07 ± 0.02ab 0.21 ± 0.06b 0.44 ± 0.14b 0.42 ± 0.12b 0.05 ± 0.02a 0.14 ± 0.04c 0.19 ± 0.05b 0.29 ± 0.07b 0.26 ± 0.06b 0.77 ± 0.17ab 1.14 ± 0.34b 0.93 ± 0.24b 70.2 ± 9.5c

Tri-2

Hergo

Tri-1

0.01 ± 0.0ab 0.13 ± 0.05a 0.02 ± 0.01ab 0.06 ± 0.02a 0.12 ± 0.04a 0.12 ± 0.03a 0.02 ± 0.01a 0.03 ± 0.01ab 0.05 ± 0.02a 0.08 ± 0.03a 0.07 ± 0.02a 0.14 ± 0.06a 0.32 ± 0.10a 0.25 ± 0.08a 47.4 ± 5.9b

Dim-3

0.96 ± 0.03ab 0.06 ± 0.01ab 0.17 ± 0.02b 0.4 ± 0.05b 0.51 ± 0.08b 0.05 ± 0.02a 0.11 ± 0.01bc 0.15 ± 0.02b 0.25 ± 0.04b 0.25 ± 0.03b 1.02 ± 0.03ab 1.15 ± 0.14b 0.81 ± 0.06b 27.4 ± 4.5a

Terhi

Dim-2

0.05 ± 0.0d

Tytti

cultivars

Table 2. PAs Content in Sea Buckthorn Purees (mg/100 g FW)a

Journal of Agricultural and Food Chemistry Article


Article

Journal of Agricultural and Food Chemistry Table 4. Sensory Attributes and Their Intensities (Scale 0−10) in the Puree Samples sensory samples

sweetness


1.2 1.1 0.9 1.1 2.0 1.6

± ± ± ± ± ±

0.7 1.0 0.9 0.9 1.0 1.1

sourness 7.5 7.3 7.4 7.2 4.8 5.7

± ± ± ± ± ±

1.7c 1.5c 1.9c 1.9c 1.6a 1.5b

bitterness 3.9 4.2 4.4 4.2 3.3 4.4

± ± ± ± ± ±

2.0 2.2 2.3 2.2 1.7 1.9

mouth-drying astringency 2.5 2.7 2.8 2.4 2.0 2.0

± ± ± ± ± ±

1.5bc 1.5c 1.6c 1.5abc 1.5a 1.2ab

puckering astringency 3.8 3.6 3.2 3.4 2.0 2.8

± ± ± ± ± ±

1.9c 1.8c 1.7bc 1.9c 1.4a 1.6b

aftertaste 4.7 4.8 4.5 4.5 3.3 3.8

± ± ± ± ± ±

1.5b 1.8b 2.0b 1.8b 1.7a 1.8a

sharpness 5.1 5.2 4.9 4.7 2.7 3.6

± ± ± ± ± ±

2.7c 2.6c 2.8c 2.9c 2.2a 2.6b

total flavor 7.3 7.0 7.3 6.8 5.1 5.9

± ± ± ± ± ±

1.4c 1.4c 1.5c 1.5c 1.7a 1.3b

Means ± standard deviations. Significant differences between sensory samples in each attribute based on three-way ANOVA together with Tukey’s post hoc test (p < 0.05) are marked with a−c.

a

role in the sensory profile of sea buckthorn puree. The puree of “Trofimovskaya” was described as the least sour and having the lowest intensities of puckering astringency and sharpness among the cultivars, whereas “Hergo” was evaluated as being the opposite in these attributes. Similarly, the puree of other cultivars, “Terhi”, “Tytti”, and “Leikora”, had higher intensities of sourness, astringency, and total flavor, whereas that of “Avgustinka” had lower score of sourness and sharpness (p < 0.05). No significant differences were detected in sweetness and bitterness (Table 4). In general, cultivars of “Trofimovskaya” and “Avgustinka” were sweeter and less sour and astringent, significantly different from the other cultivars according the scores of sensory attributes. “Hergo”, “Leikora”, “Trofimovskaya”, and “Avgustinka” were collected from the same site; thus, the genetic background was the more important factor affecting the sensory properties of sea buckthorn berry in this study. Phenolic Compounds Contributing to Sensory Properties. Two PLS regression models were created to investigate the contributions of contents of flavonol glycosides, PAs, sugars, and organic acids (X-variables, n = 40) or the corresponding ratios of the aforementioned variables (X-variables, n = 37) to various sensory characteristics (Y-variables, n = 8) in sea buckthorn puree samples (Figures 2A and B). In the model with the contents of the compounds (Figure 2A), 76% of the chemical variables explained 95% of the variation in the sensory data in the first two factors (validated R2 = 0.751). The Factor-1 in Figure 2A showed major differences among the six cultivars based on sweetness and other attributes on the first factor. All of the sugar variables excluding L-quebrachitol were located on the left side of the correlations loadings plot together with sweetness and correlated with cultivars “Avgustinka” and “Trofimovskaya” (Figure 2A). Glucose and fructose were the major sugars contributing to the sweetness in sea buckthorn purees, correlating positively with the higher pH and °Brix values. L-quebrachitol located in the middle of the PLS model and shows little correlation with the sensory attributes (Figure 2A). Organic acids and isorhamnetin glycosides as well as total PAs were located on the right side of the plot with the sourness, mouth-drying astringency, and puckering astringency (Figure 2A) associated with the cultivars “Terhi”, “Tytti”, “Leikora”, and “Hergo”. The positive correlation between astringent properties and the contents of malic acid, quinic acid, and the total acids as well as their negative correlation with pH is in accordance with previous findings showing that organic acids and pH affect not only sourness but also astringency.32−34 Various phenolic compounds, especially isorhamnetin glycosides, contributed strongly to mouth-drying astringency (Figure 2A). No clear correlation was found between bitterness and flavonols (glycosides, aglycones) or bitterness and PAs in Figure 2A. The FGs are not typically perceived as bitter,17

whereas bitter taste receptors (hTAS2R14 and hTAS2R39) can be activated by flavonol aglycones such as isorhamnetin.18 Almost all the PA variables (except dimer-2 and total PAs) and quercetin glycosides were also located in the left side of the plot (Figure 2A). Consistent with previous findings, quercetin glycoside and PA contents correlated with mouth-drying astringency in blackcurrants.20,22 Especially, quercetin-3-Orutinoside is known to induce oral astringency at extremely low concentrations in red currant juice.19 The taste recognition thresholds of quercetin compounds and procyanidins B1, B2, and B3 isolated from red wine have been detected for astringency and bitterness in water.16 Although the concentrations of quercetin glycosides were above the taste thresholds reported in water,16 the astringency was not well explained by quercetin glycoside variables in the SB puree samples. It is possible that the potential astringency of quercetin glycosides was suppressed by the higher intensity of sourness in the overall profile as a result of the high concentration of the acids.35,36 This was in accordance with previous findings showing that astringency intensity could be significantly modified by altering pH.33 It is important to note that different food matrixes may have a strong influence on the thresholds of the compounds.37 The PA dimers and trimers in red wine have been reported to be both bitter and astringent, and molecular size was the major factor influencing the sensory properties of bitterness and astringency.16,38 However, astringency and bitterness were not well explained by the PA variables in the SB puree samples. The concentrations of PAs in this study were below the values found for astringency and bitter taste thresholds of these compounds.16 It is also possible that the perception of astringency and bitterness induced by these variables was masked by sourness in the SB purees.35,39 Moreover, flavan-3-ol monomers and PAs with DP > 4 were not analyzed in this study; these compounds may have bitter properties in addition to astringent properties.16 Specifically, the flavan-3-ol monomers have bitterness stronger than that of PA dimers and trimers.38 In addition to the contents of individual sensory-active compounds, it is important to consider their relative quantities in determining the net flavor profile of food. Ratio between sugars and organic acids is often considered as a predictor of sourness and/or sweetness of berries and berry products. To study the ratios between sugars, acids, and phenolic compounds, we used the ratio variables (Supplementary Table 2) as X-variables (n = 37) in a PLS regression model to investigate their relationship with various sensory characteristics (Y-variables, n = 8) in the six purees of sea buckthorn (Figure 2B). In the model, 81% of the ratios explained 90% of the variation in the sensory data in the first two factors (validated R2 = 0.774). As shown in Figure 2B, sugar/acid ratio was a more important predictor in determining the intensities of the sweetness or sourness than the total contents of sugars or acids alone.21,40 9876


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Figure 2. PLS regression models showing the interactions between (A) chemical variables as X-variables (n = 40; blue font) or (B) ratios of chemical variables as X-variables (n = 37; blue font) and sensory profiles as Y-variables (n = 8; red font) in six puree samples (green font). Is, isorhamnetin; Qu, quercetin; G, glucoside; Rh, rhamnoside; R, rutinoside; S, sophoroside; FGs, flavonol glycosides; FAs, flavonol aglycones; Tot, total; PAs, proanthocyanidins; EG, ethyl β-D-glucopyranoside.

also reported that the ratio of bitter/sweet compounds determines bitterness perception in lettuce.41 These correlations indicated that bitterness was a complex perception related to contents of EG, sugars, acids, and phenolic compounds in the sea buckthorn berries.23,41 The ratios of phenolic compounds to sugars showed strongly positive correlation with mouth-drying astringency. Moreover, aroma-active volatiles are generally important factors in the overall flavor of a food, and they affect the perception of taste properties; for example, they may increase sweetness.42 Some aroma-active volatile compounds have been reported to influence the taste and astringent properties in the fermented SB berries.43,44 However, the bitterness and astringency are primarily caused by nonvolatile molecules rather than the aroma compounds.45 In addition to the compounds studied, other components of the puree, including volatiles, lipids, and polysaccharides in sea buckthorn berry purees, may have important roles in the sensory attributes.

Moreover, the ratios of sugars and phenolic compounds (sugars/tot PAs, sugars/tot Qu, sugars/tot Is, sugars/tot FGs, and sugars/tot FAs) correlated positively with sweetness and negatively with the other sensory variables on the first factor of the model. The ratios of acids/tot Qu (total content of quercetin aglycone) and Is/Qu (total content of isorhamnetin aglycone/total content of quercetin aglycone) correlated positively with bitterness, sharpness, sourness, after-taste, total flavor, and both types of astringency. Interestingly, the ratios of acids and variables of phenolic compounds (acids/tot Qu, acids/PA tetramers, acids/tot Is, acids/tot FAs, acids/PA timers, acids/tot FGs, and acids/PA dimers) were strongly associated with bitterness. Hence, the ratios between acids and phenolic compounds are more important factors to predict bitterness than these variables alone. We previously showed that EG is related to bitterness of sea buckthorn.23 The ratio of EG/acids correlated positively with sweetness, as shown in Figure 2B. Chadwick et al. 9877


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(3) Dueñas, M.; Muñoz-González, I.; Cueva, C.; Jiménez-Girón, A.; Sánchez-Patán, F.; Santos-Buelga, C.; Moreno-Arribas, M.; Bartolomé, B. A survey of modulation of gut microbiota by dietary polyphenols. BioMed Res. Int. 2015, 2015, 1−15. (4) Soares, S.; Brandão, E.; Mateus, N.; De Freitas, V. Sensorial properties of red wine polyphenols: astringency and bitterness. Crit. Rev. Food Sci. Nutr. 2017, 57, 937−948. (5) Ma, W.; Guo, A.; Zhang, Y.; Wang, H.; Liu, Y.; Li, H. A review on astringency and bitterness perception of tannins in wine. Trends Food Sci. Technol. 2014, 40, 6−19. (6) Laaksonen, O.; Knaapila, A.; Niva, T.; Deegan, K. C.; Sandell, M. Sensory properties and consumer characteristics contributing to liking of berries. Food Quality and Preference 2016, 53, 117−126. (7) Lesschaeve, I.; Noble, A. C. Polyphenols: factors influencing their sensory properties and their effects on food and beverage preferences. Am. J. Clin. Nutr. 2005, 81, 330S−335S. (8) Ma, X.; Laaksonen, O.; Zheng, J.; Yang, W.; Trépanier, M.; Kallio, H.; Yang, B. Flavonol glycosides in berries of two major subspecies of sea buckthorn (Hippophaë rhamnoides L.) and influence of growth sites. Food Chem. 2016, 200, 189−198. (9) Yang, B.; Halttunen, T.; Raimo, O.; Price, K.; Kallio, H. Flavonol glycosides in wild and cultivated berries of three major subspecies of Hippophaë rhamnoides and changes during harvesting period. Food Chem. 2009, 115, 657−664. (10) Zheng, J.; Kallio, H.; Yang, B. Sea buckthorn (Hippophaë rhamnoides ssp. rhamnoides) berries in Nordic environment: compositional response to latitude and weather conditions. J. Agric. Food Chem. 2016, 64, 5031−5044. (11) Hellströ m , J. K.; Tö r rö n en, A. R.; Mattila, P. H. Proanthocyanidins in common food products of plant origin. J. Agric. Food Chem. 2009, 57, 7899−7906. (12) Yang, W.; Laaksonen, O.; Kallio, H.; Yang, B. Proanthocyanidins in sea buckthorn (Hippophaë rhamnoides L.) berries of different origins with special reference to the influence of genetic background and growth location. J. Agric. Food Chem. 2016, 64, 1274−1282. (13) Kortesniemi, M.; Sinkkonen, J.; Yang, B.; Kallio, H. NMR metabolomics demonstrates phenotypic plasticity of sea buckthorn (Hippophaë rhamnoides) berries with respect to growth conditions in Finland and Canada. Food Chem. 2017, 219, 139−147. (14) Kortesniemi, M.; Sinkkonen, J.; Yang, B.; Kallio, H. H-1 NMR spectroscopy reveals the effect of genotype and growth conditions on composition of sea buckthorn (Hippophae rhamnoides L.) berries. Food Chem. 2014, 147, 138−146. (15) Yang, W.; Laaksonen, O.; Kallio, H.; Yang, B. Effects of latitude and weather conditions on proanthocyanidins in berries of Finnish wild and cultivated sea buckthorn (Hippophaë rhamnoides L. ssp. rhamnoides). Food Chem. 2017, 216, 87−96. (16) Hufnagel, J. C.; Hofmann, T. Orosensory-directed identification of astringent mouthfeel and bitter-tasting compounds in red wine. J. Agric. Food Chem. 2008, 56, 1376−1386. (17) Scharbert, S.; Holzmann, N.; Hofmann, T. Identification of the astringent taste compounds in black tea infusions by combining instrumental analysis and human bioresponse. J. Agric. Food Chem. 2004, 52, 3498−3508. (18) Roland, W. S.; van Buren, L.; Gruppen, H.; Driesse, M.; Gouka, R. J.; Smit, G.; Vincken, J. Bitter taste receptor activation by flavonoids and isoflavonoids: modeled structural requirements for activation of hTAS2R14 and hTAS2R39. J. Agric. Food Chem. 2013, 61, 10454− 10466. (19) Schwarz, B.; Hofmann, T. Sensory-guided decomposition of red currant juice (Ribes rubrum) and structure determination of key astringent compounds. J. Agric. Food Chem. 2007, 55, 1394−1404. (20) Laaksonen, O. A.; Salminen, J.; Mäkilä, L.; Kallio, H. P.; Yang, B. Proanthocyanidins and their contribution to sensory attributes of black currant juices. J. Agric. Food Chem. 2015, 63, 5373−5380. (21) Tiitinen, K. M.; Hakala, M. A.; Kallio, H. P. Quality components of sea buckthorn (Hippophae rhamnoides) varieties. J. Agric. Food Chem. 2005, 53, 1692−1699.

Our study showed that the purees prepared from berries of different sea buckthorn cultivars differ significantly in chemical composition and sensory quality. Sourness due to the high content of acids is the most dominant sensory attribute in the purees, followed by the astringent properties and bitterness. Although the conclusions in this study were made based on only six cultivars, and only some of the taste-active compounds were included, the chemical composition was able to explain the sensory quality of the purees to some extent. The present study showed malic acid and isorhamnetin glycosides were the major compounds responsible for the astringency in sea buckthorn puree, whereas some of the known astringent compounds such as proanthocyanidin dimers and trimers or quercetin glycosides showed less impact on the attributes. Moreover, the ratios between acids and phenolic compounds were more important predictors of bitterness than the variables alone. Astringency and bitterness are often the limiting factors for consumption of sea buckthorn. By understanding the relationship of chemical factors and these sensory attributes, it is possible to improve the sensory properties and consumer acceptance of sea buckthorn products, which is crucial for increasing the utilization of sea buckthorn in the food industry. This study provides important information for farmers and the food industry in selection proper cultivars for cultivation and processing.

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.jafc.7b04156. Supplementary Table 1: sensory attributes, descriptions with references, and their intensities used in sensory profiling of sea buckthorn samples; Supplementary Table 2: ratios between compounds in all sea buckthorn samples (PDF)

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AUTHOR INFORMATION

Corresponding Author

*Tel.: +358 2 333 6844; Fax: +358 2 231 7666; E-mail: baoru.yang@utu.fi. ORCID

Xueying Ma: 0000-0002-0887-2693 Wei Yang: 0000-0002-7889-6172 Funding

This work was supported by a personal grant from the China Scholarship Council (Grant 201307960009), China and the Finnish Food and Drink Industries’ Federation (ETL), Finland. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS We acknowledge Mr. Hannu Lappalainen, Mr. Bärtil Lappalainen, Mr. Seppo Lappalainen, and Ms. Hedi Kaldmäe for providing the sea buckthorn berries.

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REFERENCES

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