Influence of ripening stage on bioactive compounds and antioxidant activity in nine fig (Ficus carica L.) varieties grown in Extremadura, Spain

Influence of ripening stage on bioactive compounds and antioxidant activity in nine fig (Ficus carica L.) varieties grown in Extremadura, Spain

Journal of Food Composition and Analysis 64 (2017) 203–212 Contents lists available at ScienceDirect Journal of Food Composition and Analysis journa...

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Journal of Food Composition and Analysis 64 (2017) 203–212

Contents lists available at ScienceDirect

Journal of Food Composition and Analysis journal homepage: www.elsevier.com/locate/jfca

Original research article

Influence of ripening stage on bioactive compounds and antioxidant activity in nine fig (Ficus carica L.) varieties grown in Extremadura, Spain

MARK



Cristina Pereiraa,b, Margarita López-Corralesa, Manuel Joaquín Serradillac, , María del Carmen Villalobosb,d, Santiago Ruiz-Moyanob,d, Alberto Martínb,d a

Centro de Investigación Finca La Orden-Valdesequera (CICYTEX), Área de Hortofruticultura, Junta de Extremadura, Autovía Madrid-Lisboa s/n, 06187, Badajoz, Spain Instituto Universitario de Investigación en Recursos Agrarios (INURA), Avda. de de la Investigación s/n, Campus Universitario, 06006, Badajoz, Spain c Instituto Tecnológico Agroalimentario de Extremadura (INTAEX-CICYTEX). Área de Vegetales, Junta de Extremadura, Avda. Adolfo Suárez s/n, 06007, Badajoz, Spain d Nutrición and Bromatología, Escuela de Ingenierías Agrarias, Universidad de Extremadura, Avda. Adolfo Suárez s/n, 06007, Badajoz, Spain b

A R T I C L E I N F O

A B S T R A C T

Keywords: Ficus carica Ripening Skin Flesh Food composition Food analysis Phytochemicals Antioxidant capacity

The aim of this study was to characterise nine commercial fig (Ficus carica L.) varieties differing in colour (darkpurple, brown, green, and yellow-green) at three different ripening stages in regards to the health-promoting compounds of their fruits and to identify and quantify the bioactive compounds as well as total antioxidant activity (TAA) in the skin and flesh of each variety. Significant differences (p < 0.05) were found between varieties and ripening stages. Dark-coloured varieties showed the highest levels of total phenolic compounds (from 26.7 to 169.5 mg gallic acid equivalents/100 g), quercetin-3-O-rutinoside (between 4.6 and 11.9 mg/ 100 g), and anthocyanins, specially cyanidin-3-O-rutinoside (from 3.03 to 97.4 mg/100 g), while brown-, green-, and yellow-green-coloured varieties contained the highest levels of chlorogenic acid (between 0.7 and 2.1 mg/ 100 g), total Vitamin C (from 0.8 to 9.0 mg/100 g), and (+)-catechin as proanthocyanin cleavage products (from 3.1 to 17.3 mg/100 g). Levels of TAA were measured by 2,2′-azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) diammonium salt (ABTS) total radical scavenging capacity both in hydrophilic (H-TAA) and lipophilic (LTAA) fractions. The darker varieties exhibited higher H-TAA values, ranging from 16.3 to 177.4 mmol Trolox equivalents/100 g, than the lighter ones. In the case of L-TAA, its concentration also depended directly on the genotype and less on the ripening stage. We found higher concentrations of bioactive compounds and a higher antioxidant capacity in the skin compared to the flesh; moreover, their content increased during the ripening process, reaching the maximum level of phenolic compounds at stage three, although these changes were deeper in the dark-coloured varieties and in the brown-coloured variety ‘San Antonio’ Based on our results, it is advisable to consume unpeeled, fully ripe, dark figs in order to optimally benefit from the health-promoting properties.

1. Introduction

and more susceptible to postharvest disorders (Villalobos et al., 2016). Figs are an important component of the balanced Mediterranean diet due to their high nutritional value (Crisosto et al., 2011; Solomon et al., 2006). They are a rich source of minerals, vitamins and dietary fibre (Veberic et al., 2008). Similar to other fruits, figs are rich in sugars (Crisosto et al., 2011), mainly glucose and fructose, and organic acids, but free of sodium and fat (Crisosto et al., 2010; Genna et al., 2008; Veberic et al., 2008; Veberic and Mikulic-Petkovsek, 2016). In addition, figs also have health-promoting compounds such as phenolic acids and flavonoids, including anthocyanins, proanthocyanidins, flavonols, and flavanones. These substances are related to their antioxidant potential (Crisosto et al., 2011; Solomon et al., 2006; Tanwar et al., 2014; Vallejo et al., 2012; Veberic et al., 2008) and contribute not only to improved

In recent years, the intake of fruit and vegetables has been increasing due to consumers associating their consumption with a reduced risk of major diseases and a possibly delayed onset of age-related disorders (Vicente et al., 2009). Figs (Ficus carica L.) are a seasonal food and can be consumed either fresh (peeled or unpeeled) or dried (Veberic et al., 2008). Generally, although they are considered as climacteric fruit, figs for fresh consumption should be harvested when they are almost fully ripe and have developed their optimum organoleptic characteristics (Crisosto et al., 2011). However, figs have a limited postharvest lifespan and are therefore usually harvested unripe for long-term storage, since at the optimal ripening stage, they may be soft



Corresponding author. E-mail addresses: [email protected], [email protected] (M.J. Serradilla).

http://dx.doi.org/10.1016/j.jfca.2017.09.006 Received 2 March 2016; Received in revised form 28 August 2017; Accepted 15 September 2017 Available online 18 September 2017 0889-1575/ © 2017 Elsevier Inc. All rights reserved.

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each block and variety were grouped into three ripening stages, based on texture and skin colour, using a TA.XT2i Texture Analyzer (Stable Micro Systems, Godalming, UK) and a CR-400 tristimulus colorimeter (Minolta, Tokyo, Japan) respectively, and without visual defects. In all cases, ripening stage two corresponded to the ripening stage of fruits because the fruit flesh gave in slightly when touched, while ripening stage one corresponded to a stage less unripe, with firmer fruits. Ripening stage three corresponded to tree-ripe or fully ripe and therefore softer fruits than those commercially available but not overripe. Total and individual phenolic compounds, total vitamin C, and 2,2′azino-bis(3-ethylbenzothiazoline-6-sulphonic acid) diammonium salt (ABTS) total radical scavenging capacity were determined using three replicates of ten healthy fruits from a homogeneous sample of each ripening stage and variety. Fruit peel and flesh were separated. All samples were packed in plastic bags, frozen and stored at −80 °C until analysis.

human health, but also to the good quality of the fruit, since they have a great impact on colour, flavour, and sensory properties such as bitterness and astringency (Lee, 2000; Piga et al., 2008). The concentration of these compounds in fruits is strongly influenced by genotype, ripening stage, and weather conditions (Crisosto et al., 2011; Solomon et al., 2006; Çalişkan and Polat, 2011). The health promoting properties of figs have resulted in several studies about their polyphenol content and antioxidant activity (Solomon et al., 2006; Veberic et al., 2008; Dueñas et al., 2008; Vallejo et al., 2012), as well as their functional properties. For instance, Vinson et al. (2005) reported that fig antioxidants could protect plasma lipoproteins from oxidation and induced a significant increase in the antioxidant capacity of plasma 4 h after consumption. To date, to the best of our knowledge, there are no studies on the accumulation of bioactive compounds during the ripening process of figs. Notwithstanding, one study (Crisosto et al., 2010) examined the influence of two different ripening stages on the antioxidant capacity of four fresh fig cultivars. Moreover, previous studies have examined the influence of genotype and harvest season on phenolic content (Valero and Serrano, 2010; Veberic and Mikulic-Petkovsek, 2016). Most authors have focused on the identification of anthocyanins and polyphenols present in figs of different varieties grown in Slovenia, Israel, Italy, and Spain, as well as in their distribution or quantification in the fruit skin and flesh (Veberic et al., 2008; Solomon et al., 2006; Piga et al., 2008; Dueñas et al., 2008; Vallejo et al., 2012), but not during the process of ripening. Therefore, the objective of this study was to evaluate the impact of different ripening stages on the content of health-promoting compounds and antioxidant capacity in nine fig varieties.

2.2. Total phenolic (TP) content

2. Materials and methods

Phenolic compounds were extracted and determined from 5 g of skin and flesh from figs of each variety and ripening stage, following the method described by Lima et al. (2005). Thirty mL of solvent (80% aqueous ethanol, containing 1% conc. HCl) were added, and the sample was extracted using a magnetic mixer for 20 min in the absence of light at room temperature (25 °C) and subsequently filtered. The extraction process was repeated three times to obtain a totally discoloured extract and the resulting ethanolic extracts were combined to a final volume of 100 mL. Total phenolic content was measured spectrophotometrically at 760 nm using Folin-Ciocalteu reagent, with gallic acid as a standard. Results were expressed as mg of gallic acid equivalents per 100 g of fresh weight (FW).

2.1. Plant material

2.3. Total vitamin C content

This study was conducted using nine fig varieties grown in an experimental orchard located at an altitude of 217 m above sea level at the research centre “Finca La Orden-Valdesequera”, belonging tothe Scientific and Technological Research Centre of Extremadura (CICYTEX) (WGS −89, latitude 38° 51 7.78” N, longitude 6° 40′ 16.59” W), Guadajira, Badajoz, Spain. The following fig varieties were studied: green-, and yellowgreen–coloured ‘Cuello Dama Blanco’ (CDB) (also known as ‘Kadota’), ‘Tres Voltas L’Any’ (TV), ‘Banane’ (BN), and ‘Blanca Bétera’ (BB) whose colour values ranged between 60.8 and 65.6 for L*, 33.5 and 47.6 for C* and 93.6 and 98.7 for hue*; brown-coloured ‘Brown Turkey’ (BT) and ‘San Antonio’ (SA) fluctuated between 51.2 to 57.3 for L*, 29 to 32 for C* and 73.6 to 76.1 for hue*; dark-coloured ‘Cuello Dama Negro’ (CDN), ‘Colar Elche’ (CE) (also known as ‘Black Mission’) and ‘De Rey’ (DR) varied from 29.8 to 35.7 for L*, 3.4 to 24.5 for C* and 86.7 to 256.4 for hue*. Regarding flesh colour, ‘Cuello Dama Blanco’ (CBD), ‘San Antonio’ (SA) and ‘De Rey’ (DR) showed an amber colour (L* = 46.6–50.7; C*: 25.6-26.5; hue* = 46.2–73.2), while ‘Blanca Bétera’ (BB), ‘Brown Turkey’ (BT), ‘Cuello Dama Negro’ (CDN) and ‘Colar Elche’ (CE) were characterised by a pink colour (L*: 46.6–57.8; C* = 22.3–27.1 and hue*: 46.2 and 63.5. Finally, ‘Tres Voltas L’Any’ (TV) and ‘Banane’ (BN) showed a red colour, ranging from 49.8 to 51.5 for L*, from 22.3 to 22.5 for C* and from 52.4 to 57.4 for h*. All evaluated varieties are considered ‘Common type’ and produce figs parthenocarpically. The plant material originated from cuttings obtained from the National Fig Germplasm Bank located in CICYTEX. The varieties were selected based on fruit quality traits such us skin colour and flesh firmness for fresh consumption. The experimental design of this trial consisted of four randomised blocks (three trees per block) with a planting density of 5 m × 4 m. Fig samples were collected randomly from three trees of each block for each variety in a single harvest during one growing season (2012). After harvesting, the fruits from

Total vitamin C was analysed as ascorbic acid (AA) and dehydroascorbic acid (DHA) content. Extraction and determination AA and DHA were conducted according to the methods described by Fernández-León et al. (2013), based on Zapata and Dufour (1992), with some modifications (Gil et al., 1999). Briefly, 10 g of skin or flesh of each sample were homogenised with 10 mL of a methanol/water mixture (5:95), containing citric acid (21 g/L) and EDTA (0.5 g/L). The homogenate was filtered through a cheesecloth and a C18 Bakerbond SPE column (Waters, Milford, MA, USA). The analysis was performed in an Agilent model 1200 Series liquid chromatograph (HPLC) with a diode array detector (DAD) (Agilent Technologies, Palo Alto, CA, USA) after derivatisation of DHA into fluorophore 3-(1,2-dihydroxyethyl) furol [3,4-b] quinoxaline-1-one (DFQ), with 1,2-phenylenediamine dihydrochloride (OPDA). Total vitamin C was expressed as the sum of AA and DHA (mg) per 100 g of FW. 2.4. Antioxidant activity 2.4.1. ABTS total radical scavenging capacity The 2,2-azino-bis-(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS) radical scavenging assay was performed based on the procedure described by Cano et al. (1998). It allows determination of total antioxidant activity (TAA) due to both hydrophilic (HTAA) and lipophilic (L-TAA) compounds in the same extraction. Hydrophilic and lipophilic compounds were extracted using the method described by Serrano et al. (2009). Briefly, 5 g of skin and flesh tissue of each sample were homogenised in 10 mL of 50 mM phosphate buffer, pH 7.8, and 6 mL ethyl acetate and centrifuged. The upper fraction was used for analysing L-TAA, while H-TAA was measured in the lower fraction, using an enzymatic system composed of ABTS, horseradish peroxidase enzyme (HRP), and its oxidant substrate (hydrogen peroxide). From each homogenate, 20 μL of juice were placed in a 204

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spectrometer cuvette and 1 mL of the radical cation, 0.730 mmol L−1 ABTS+%, was added. The initial absorbance value at 730 nm was compared with the absorbance obtained after a reaction time of 20 min. Trolox, a water-soluble vitamin E analogue, was used as a standard. Results were expressed as mmol Trolox equivalents per 100 g of FW.

levels of TP. Additionally, TP concentrations were 70–83% higher in the skin than in the flesh. On the other hand, fruits at ripening stage three also had higher levels than fruits at stage one (Figs. 1 and 2). Variety CDN showed the highest TP content in both skin and flesh, with 169.5 and 34.3 mg of gallic acid equivalents per 100 g of FW, respectively, whilst CDB showed the lowest TP content with 58.9 mg of gallic acid equivalents per 100 g of FW for skin and 23.3 mg of gallic acid equivalents per 100 g of FW for flesh. Çalişkan and Polat (2011) studied a total of 76 different accessions and also observed a large diversity in TP levels, ranging from 28.6 (‘Bakrasi’) to 211.9 mg of gallic acid equivalents per 100 g in the flesh (‘Siyak 5′). In addition, our study is in agreement with similar studies which reported higher TP levels in the skin than in the flesh (Piga et al., 2008; Solomon et al., 2006; Vallejo et al., 2012). Despite similar weather conditions, TP levels in our study were considerably higher than those reported by Vallejo et al. (2012), which suggests a strong influence of the factors genotype and ripening stage on TP values, regardless of climatic conditions. Additionally, this study confirmed the influence of the interaction factor ‘variety × stage’ on TP levels since this interaction was statistically significant both in skin and flesh. Data are provided in the Supplementary material (Tables S1 and S2). Very few studies have determined and quantified total phenolic content in figs or cash crops during the ripening process; the results of our study are similar to those obtained from similar studies using mainly stone fruits (Serradilla et al., 2011; Valero and Serrano, 2010).

2.5. Individual phenolic compounds Identification and quantification of individual phenolic compounds and anthocyanins was carried out according to Vallejo et al. (2012). The method was slightly modified, which enabled determination of both phenolic compounds and oligomeric proanthocyanidins depolymerised in the presence of phloroglucinol (phloroglucinolysis). For the extraction of anthocyanins and phenolic compounds, 10 g of flesh and 5 g of skin from each variety and ripening stage were homogenised. Then, 40 mL of extraction solution (acetone/formic acid; 95/5, v/v) were added to each of the three replicates. Supernatants were concentrated under vacuum and filtered through a C18 Sep-Pak cartridge (Waters Corp, Milford, MA, USA). Subsequently, the samples (50 μL) were analysed on an Agilent liquid chromatograph model 1100 Series (Agilent Technologies, Palo Alto, CA, USA), using DAD/FLD/ESI–MS detectors. Separations were achieved using a Gemini-NX C18 column (150 × 4.6 mm i.d., 5 μm, Phenomenex, Torrance, CA, USA). The mobile phase was a mixture of water-formic acid (95:5 for VWR-Merck and 98:2 for Agilent, v/v) (A) and methanol (B). The flow rate was 1 mL/ min at a linear gradient, with 5% B at 5 min, 8% B at 10 min, 13% B at 15 min to reach 15% B at 19 min, 40% B at 47 min, 65% B at 64 min, and 98% B at 69 min. Chromatograms were recorded at 280, 320, 360, and 510 nm. Identification of compounds was carried out by comparing their retention times and UV spectra with those of pure commercial standards. Its quantification was assessed from peak areas and calculated as equivalents of these standards, using linear regression curves for each standard. The results were expressed as mg per 100 g of FW. The depolymerisation procedure using phloroglucinol was performed with 100 mg of skin and 50 mg of flesh from each sample. At the start of the reaction, we added 1.6 mL of phloroglucinol solution as described by Vallejo et al. (2012). Samples (10 μL) were analysed by the reversed phase on the same HPLC–ESI–MS in negative mode. The mobile phase was a water-acetic acid (97.5:2.5 v/v) (A) and acetonitrile (B) mixture. The flow rate was 1 mL/min and the following gradient was applied, starting with 3% B, 9% B linear gradient at 5 min, 16% B linear at 15 min, to reach 50% B at 45 min, followed by washing and reconditioning of the column with 3% B at 52 min up to 57 min. A chromatogram was recorded at 280 nm, and calibration curves were obtained using pure standards. Results were expressed as mg per 100 g of FW.

3.2. Total vitamin C contents of skin and flesh at different ripening stages Total vitamin C content was determined as the sum of ascorbic acid (AA) and its oxidation product, dehydroascorbic acid (DHA), in skin and flesh of fig fruits at different ripening stages (Figs. 1 and 2; Tables S1 and S2). Vitamin C is considered as the most widely distributed water-soluble antioxidant in vegetables (Oliveira et al., 2009). Variety BN showed the highest total vitamin C content in both skin and flesh, with 9.0 mg and 5.0 mg of total vitamin C per 100 g of FW, respectively. These values were between two and four times higher than those described for figs, around 2 mg per 100 g of FW (National Nutrient Database, USDA, 2016). Total vitamin C content of the skin did not differ between ripening stages. However, at the flesh level, total vitamin C levels decreased significantly from stage one to stage two and then progressively increased until stage three (Tables S1 and S2). Similar behaviour has been described by Serradilla et al. (2017)for ascorbic acid in sweet cherries during the ripening process. The biosynthesis and accumulation of vitamin C depend mainly on different maturation models followed by different species (Valero and Serrano, 2010), although climatic conditions and cultural practices have a significant influence on the final vitamin C concentration (Lee and Kader, 2000). According to Valero and Serrano (2010), this could be explained by oxidation processes throughout the ripening process. For instance, at the beginning of ripening, hydrogen peroxide is produced to reach the organoleptic characteristics of mature fruit. Here, ascorbic acid plays an important role in overseeing this radical turnover during fruit ripening. Apart from environmental conditions and cultural practices, the interaction factor ‘variety × stage’ was significant both in skin and flesh (Tables S1 and S2), showing a strong influence of the genotype and ripening stage on total vitamin C content. Lee and Kader (2000) also concluded that the selection of the genotype is the main factor to consider when high vitamin C concentrations are desired.

2.6. Statistical analysis Statistical analysis was carried out using SPSS for Windows, version 19.0 (SPSS Inc., Chicago, IL, USA). Functional composition and ABTS total radical scavenging capacity were examined by analysis of variance (ANOVA), with ‘variety’ and ‘ripening stage’ as dependent betweensubject factors. For the comparison of mean values, Tukey’s honestly significant difference (HSD) test (p ≤ 0.05) was performed. The relationships among the parameters studied were evaluated via principal components analysis (PCA). 3. Results and discussion 3.1. Total phenolic content in skin and flesh at different ripening stages

3.3. ABTS total radical scavenging capacityin skin and flesh at different ripening stages

Total phenolic (TP) content was determined for each variety, tissue type, and ripening stage (Figs. 1 and 2). High levels of TP were found in dark-coloured varieties such as CDN and CE. The varieties CDB and BB, with yellow-green and green fruit skin colours, showed much lower

Total antioxidant activity (TAA) of both skin and flesh of figs was determined using ABTS assays in both hydrophilic (H-TAA) and lipophilic (L-TAA) fractions, since the presence of lipophilic compounds, such as carotenoids, and hydrophilic compounds, such as flavonoids 205

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Fig. 1. Mean values (n = 9 for variety and n = 27 for ripening stage) of total phenolic content (TP), total vitamin C, hydrophilic (H-TAA) and lipophilic (L-TAA) fractions for each variety and ripening stage at skin level.

Fig. 2. Mean values (n = 9 for variety and n = 27 for ripening stage) of total phenolic content (TP), total vitamin C, hydrophilic (H-TAA) and lipophilic (L-TAA) fractions for each variety and ripening stage at flesh level.

Petkovsek, 2016), skin is the major tissue contributing to TAA and, for this reason, it is advisable to consume whole figs instead of peeled fruits, as the skin is an excellent source of health-promoting compounds. Again, dark-coloured varieties, such as CE and CDN with 177.4 and 109.4 mmol Trolox equivalents per 100 g of FW, respectively, showed the highest TAA levels. Solomon et al. (2006) and Crisosto et al. (2010) also reported higher antioxidant activities in extracts of dark fig

and vitamins, contribute to the total antioxidant activity of fruits and vegetables (Valero and Serrano, 2010). In all varieties, H-TAA was higher than L-TAA in both skin and flesh samples. Consequently, TAA values of the skin were between two and ten times higher than in the flesh, depending on the variety (Figs. 1 and 2). According to our results and taking into account previous studies (Çalişkan and Polat, 2011; Solomon et al., 2006; Vallejo et al., 2012; Veberic and Mikulic206

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Table 1 Anthocyanin content in skin and flesh for the varieties ‘De Rey’, ‘Cuello Dama Negro’, ‘Colar Elche’, San Antonio’, and ‘Brown Turkey’ at each ripening stage. Variety/Stage

Cyanidin-3-O-glucoside Mean

Cyanidin-3-O-rutinoside

Max

Pelargonidin-3-O-rutinoside

Min

Mean

Max

Min

Mean

Max

Min

Fruit skin (mg/100 g) Variety1 ‘BT' ‘SA' ‘DR' ‘CDN' ‘CE'

0.13c 0.12c 6.39a 3.31b 2.78b

0.25 0.19 12.79 6.75 6.94

0.06 0.09 3.41 0.46 1.70

27.5c 12.19c 34.03c 97.4a 74.25b

67.45 18.41 59.27 135.49 181.66

7.84 6.56 13.38 38.69 20.57

0.14c 0.09c 5.64a 1.79b 2.8b

0.37 0.11 9.40 2.92 5.60

0.02 0.06 2.04 0.89 0.41

Stage 1 2 3 p variety2 p stage p variety* stage

1.64b 2.26b 3.74a *** *** ns

5.78 8.09 12.79

0.06 0.11 0.09

32.66b 39.39b 75.18a *** *** ***

91.87 123.25 181.66

7.84 6.56 11.28

1.43a 2.24ab 2.61b *** * ns

4.91 8.00 9.40

0.02 0.09 0.08

Fruit flesh (mg/100 g) Variety ‘BT' ‘SA' ‘DR' ‘CDN' ‘CE'

0.01c 0.02c 0.66a 0.4b 0.28b

0.02 0.03 0.83 0.83 0.43

0.01 0.02 0.43 0.23 0.16

1.82bc 1.21c 3.03b 5.92a 5.43a

4.82 2.09 4.86 10.50 7.50

0.86 0.79 1.13 4.05 4.07

0.01c 0.02c 0.09ab 0.21ab 0.26a

0.01 0.03 0.41 1.07 0.65

0.00 0.01 0.04 0.06 0.18

Stage 1 2 3 p variety2 p stage p variety*stage

0.26a 0.27a 0.29a *** ns ns

0.72 0.83 0.83

0.01 0.01 0.01

3.17a 3.41a 3.87a *** ns ns

6.76 7.90 10.50

0.79 1.14 0.92

0.07a 0.14a 0.15a ** ns ns

0.18 1.07 0.65

0.00 0.00 0.00

Data were presented as a mean value of 9 replicates for variety and 27 for ripening stage. BT: ‘Brown Turkey’; SA: ‘San Antonio’; DR: ‘De Rey’; CDN: ‘Cuello Dama Negro’ and CE: ‘Colar Elche’. 1 In each column, different letters indicate a significant difference at p < 0.05. 2 p values: * (p < 0.05); ** (p < 0.01); *** (p < 0.001). Table 2 Flavonol, phenolic acid, and proanthocyanin content of fruit skin for each variety and ripening stage. Variety/Stage

Flavonols

Phenolic acids

Quercitin-3-O-rutinoside Mean Max Min Concentration (mg/100 g) Variety1 ‘CDB' 3.2d ‘BB' 2.9d ‘BN' 3.2d ‘TV' 3.6d ‘BT' 3.6d ‘SA' 5.4c ’DR' 4.6cd ‘CDN' 8.9b ‘CE' 11.9a Stage 1 2 3 p variety2 p stage p variety*stage

2.7c 5.5b 7.6a *** *** ***

Proanthocyanins

Quercitin −3-acetylglucoside Mean Max Min

Chlorogenic acid Mean Max Min

Ellagic acid Mean Max

Min

Epicatechin Mean Max

Min

Catechin Mean Max

Min

4.9 4.8 9.6 5.9 8.9 8.5 6.7 16.2 16.3

1.0 0.9 0.6 1.1 1.8 1.4 1.4 5.1 5.6

1.1d 0.9d 0.8d 1.5cd 3.7a 2.7b 3.6a 2.1bc 2.1bc

1.8 1.8 1.5 3.3 4.5 6.4 4.4 3.3 3.3

0.6 0.4 0.4 0.7 2.8 0.3 1.3 1.3 1.1

1.7ab 2.0a 1.9a 2.1a 1.8ab 1.4b 0.6c 0.7c 0.7c

2.1 2.6 2.3 2.5 2.1 2.2 1.5 1.1 1.1

1.0 1.5 1.5 1.5 1.3 1.0 0.2 0.3 0.4

1.8c 1.7c 1.7c 1.7c 2.7a 2.7a 2.1bc 2.1b 2.0bc

2.1 1.9 1.8 1.8 3.3 3.3 2.8 2.5 2.2

1.6 1.5 1.6 1.6 2.2 2.1 1.6 1.8 1.8

4.8f 8.6c 5.8de 6.6de 7.0d 15.2b 5.9de 16.9a 5.0ef

6.4 11.7 7.2 7.6 10.5 20.2 7.2 25.7 7.2

3.5 5.8 4.5 5.3 4.8 12.2 4.8 10.5 3.8

12.6b 7.6c 16.5a 17.3a 8.8c 8.6c 5.1d 4.5d 9.5c

15.2 12.8 20.6 19.9 11.9 14.7 7.9 5.8 16.7

10.0 4.8 6.4 5.3 2.2 13.6 7.0 13.9 4.8

6.9 15.3 16.3

0.6 1.0 3.1

1.5a 1.9b 2.8c *** *** ***

4.4 4.5 6.4

0.3 0.4 0.8

1.3b 1.5a 1.6a *** ** ns

2.6 2.3 2.5

0.2 0.5 0.3

1.9b 1.9b 2.2a *** * ns

3.1 2.9 3.3

1.5 1.6 1.6

7.3b 7.9b 10.0a *** *** ***

14.8 16.2 25.7

4.0 3.8 3.5

9.2b 9.8b 11.2a *** *** ***

18.3 17.7 20.6

2.0 3.1 4.9

Data were presented as a mean value of 9 replicates for variety and 27 for ripening stage. CDB: ‘Cuello Dama Blanco’;BB: ‘Blanca Bétera’; BN: ‘Banane’, TV: ‘Tres Voltas L’Any’; BT: ‘Brown Turkey’; SA: ‘San Antonio’; DR: ‘De Rey’; CDN: ‘Cuello Dama Negro’ and CE: ‘Colar Elche’. 1 In each column, different letters indicate a significant difference at p < 0.05. 2 p values: * (p < 0.05); ** (p < 0.01); *** (p < 0.001).

varieties. With regard to flesh, H-TAA values were higher for the varieties TV, CDN, DR, and BN (Fig. 2), in which the flesh is characterised by a red colour. These results underline the importance of

anthocyanins, pigments responsible for the red, blue, and purple colours of many fruits (Vicente et al., 2009). Our findings are consistent with those of Çalişkan and Polat (2011), who found a highly positive 207

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Table 3 Flavonol, phenolic acid, and proanthocyanin content of fruit flesh for each variety and ripening stage. Variety/Stage

Flavonols Quercitin-3-O-rutinoside

Quercitin-3-acetylglucoside

Chlorogenic acid

Mean Concentration (mg/100 g) Variety1 ‘CDB' 0.3c ‘BB' 0.3c ‘BN' 0.3 ‘TV' 0.4bc ‘BT' 0.5bc ‘SA' 0.8ab ‘DR' 0.1c ‘CDN' 1.0a ‘CE' 1.0a Stage 1 2 3 p variety2 p stage p variety*stage

Phenolic acids

0.3b 0.6a 0.7a *** *** *

Proanthocyanins Ellagic acid

Epicatechin

Catechin

Max

Min

Mean

Max

Min

Mean

Max

Min

Mean

Max

Min

Mean

Max

Min

Mean

Max

Min

0.4 0.4 0.8 0.7 1.0 1.8 0.2 1.9 1.9

0.1 0.3 0.1 0.3 0.3 0.1 0.1 0.3 0.3

0.5a 0.6a 0.6a 0.6a 0.6a 0.6a 0.6a 0.5a 0.5a

1.2 1.2 1.2 1.2 1.2 1.2 1.0 1.3 1.4

0.2 0.3 0.2 0.1 0.3 0.2 0.1 0.1 0.1

0.9ab 0.8ab 0.7b 0.7 0.9a 0.8ab 0.1c 0.1c 0.1c

1.4 1.0 0.7 0.8 1.3 1.1 0.1 0.2 0.2

0.6 0.7 0.6 0.7 0.7 0.5 0.1 0.1 0.1

0.8b 0.8b 0.7b 0.7b 0.9b 1.0a 0.8b 0.8b 0.8b

0.9 0.9 0.8 0.8 0.9 1.4 0.9 0.9 0.8

0.7 0.8 0.7 0.7 0.8 0.8 0.8 0.8 0.7

2.4c 4.5b 2.4c 2.4c 2.2c 6.8a 2.9c 7.2a 2.7c

3.1 6.2 3.2 2.8 2.6 11.9 3.5 13.3 4.0

1.8 1.4 1.9 1.9 1.6 3.0 2.3 4.1 1.8

4.4bc 3.1d 4.8b 5.8a 3.4cd 3.8bcd 2.9de 2.0e 4.7b

6.1 5.0 5.6 7.1 4.1 6.7 3.5 2.4 5.4

3.3 1.6 3.9 4.3 1.4 3.9 4.2 1.4 1.6

0.7 1.9 1.8

0.1 0.1 0.1

0.3c 0.5b 0.9a ns *** ns

0.8 1.4 1.2

0.1 0.1 0.5

0.5a 0.5a 0.6a *** ns ns

1.1 1.4 1.3

0.1 0.1 0.1

0.8a 0.8a 0.8a *** ns ns

1.4 1.1 1.0

0.7 0.7 0.7

3.1b 3.5b 4.5a *** *** **

7.1 6.3 13.3

1.4 1.8 2.1

3.8a 3.7a 4.1a *** ns *

7.1 6.7 6.7

1.6 1.5 1.4

Data were presented as a mean value of 9 replicates for variety and 27 for ripening stage. CDB: ‘Cuello Dama Blanco’;BB: ‘Blanca Bétera’; BN: ‘Banane’, TV: ‘Tres Voltas L’Any’; BT: ‘Brown Turkey’; SA: ‘San Antonio’; DR: ‘De Rey’; CDN: ‘Cuello Dama Negro’ and CE: ‘Colar Elche’. 1 In each column, different letters indicate a significant difference at p < 0.05 2 p values: * (p < 0.05); ** (p < 0.01); *** (p < 0.001).

groups of phenolic compounds in figs are phenolic acids and flavonoids, such as anthocyanins, flavonols, and flavan-3-ols. In the case of anthocyanins (Table 1; Fig. S1), the main anthocyanin identified in our study was cyanidin-3-O-rutinoside; its concentration ranged from 12.19 (SA) to 97.4 (CDN) mg per 100 g of FW for skin and from 1.21 (SA) to 5.92 (CDN) mg per 100 g of FW. The second anthocyanin identified was cyanidin-3-O-glucoside, ranging from 0.12 (SA) to 6.39 (DR) mg per 100 g of FW for skin and from 0.01 (BT) to 0.66 (DR) for flesh. Finally, pelargonidin-3-O-rutinoside was identified as the third anthocyanin; its content fluctuated between 0.09 (SA) and 5.64 (DR) mg per 100 g of FW for skin and between 0.01 (BT) and 0.21 (DR) mg per 100 g of FW for flesh. Our results are in agreement with previous studies on anthocyanins in figs (Dueñas et al., 2008; Solomon et al., 2006; Vallejo et al., 2012; Veberic et al., 2008; Veberic and Mikulic-Petkovsek, 2016). In addition, significant differences in phenolic compounds between varieties have also been found by Dueñas et al. (2008) and Solomon et al. (2006) and are due to the grade of expression of genes controlling the anthocyanin pathway. Generally, we measured higher cyanidin-3O-glucoside and pelargonidin-3-O-rutinoside values both in skin and flesh than the authors of a similar study (Veberic and MikulicPetkovsek, 2016). However, these authors also reported higher concentrations of cyanidin-3-O-glucoside in flesh, reaching levels of 9.5 mg per 100 g of FW, which are 14 times higher than those observed in our study. The phenolic compounds identified in our study were phenolic acids such as chlorogenic and ellagic acids, flavonols such as quercetin-3-Orutinoside, and quercetin-3-acetylglucoside. Proanthocyanidins were quantified as monomers of (+)-catechin and (−)-epicatechin after an additional analysis using acid catalysis in the presence of excess phloroglucinol (phloroglucinolysis), according to the methodology described in Vallejo et al. (2012) (Tables 2 and 3). Regarding phenolic acids, chlorogenic acid values ranged from 0.6 to 2.1 mg per 100 g of FW for skin and from 0.1 to 0.9 mg per 100 g of FW for flesh. Chlorogenic acid values were always higher in the skin than in the flesh. These findings are consistent with those of Vallejo et al. (2012), although these authors found higher overall chlorogenic acid levels. In the present study, significant differences were found between varieties and ripening stages. High amounts of chlorogenic acid were noted in

correlation between TAA and anthocyanin concentration in figs. H-TAA levels measured in our study were higher than those described in a similar study by Veberic and Mikulic-Petkovsek (2016). Regarding L-TAA, we found significant differences between brown-, green-, and yellow-green −coloured and dark-coloured varieties both in skin and flesh (Figs. 1 and 2). In the skin, varieties CDB, BT, BN, CE and TV showed the highest levels of L-TAA, ranging from 8.9 to 13.3 mmol Trolox equivalents per 100 g of FW, although differences between the varieties were not significant (Tables S1 and S2). For the flesh, the varieties BN and CE showed significantly higher L-TTA levels than other varieties. The results of our study represent the first published data describing L-TAA values in figs; hence, our data cannot be compared to the findings of other studies. According to Díaz-Mula et al. (2008) and Valero et al. (2011), L-TAA levels are positively correlated with total carotenoids, pigments responsible for the yellow orange-red and red colours of many fruits, including figs (Veberic and MikulicPetkovsek, 2016). Therefore, the varieties BN and CE may potentially contain high levels of carotenoids in their flesh. During the ripening process, significant differences were only found in H-TAA levels in skins. In general, an increase in H-TAA and L-TAA, except L-TAA of flesh, was observed from stage one (55.4 mmol Trolox equivalents per 100 g of FW) to stage three (82.8 mmol Trolox equivalents per 100 g of FW). A similar tendency has been found by Crisosto et al. (2010), who also reported that the highest antioxidant capacity was reached in fully ripe figs, although there were no significant differences between ripening stages. On the other hand, H-TAA was significantly influenced by the factors ‘variety’ and the interaction ‘variety × stage’ both in skin and flesh. Nevertheless, L-TAA, according to the results obtained in this study, was only influenced by the factor ‘variety’ (Tables S1 and S2). 3.4. Phenolic compounds in skin and flesh at different ripening stages Phenolic compound content of the skin and flesh of different fig varieties was determined using HPLC-DAD/ESI–MS; the results are presented in Table 1-3. Most previous studies on figs (Dueñas et al., 2008; Solomon et al., 2006; Vallejo et al., 2012; Veberic et al., 2008; Veberic and Mikulic-Petkovsek, 2016) have reported that the two main 208

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Fig. 3. Loading plot and score plot after principal components analysis of the variables and individuals in the plane by two first principal components (PC1 and PC2) in skin. CDB1: ‘Cuello Dama Blanco’ at ripening stage 1; CDB2: ‘Cuello Dama Blanco’ at ripening stage 2; CDB3: ‘Cuello Dama Blanco’ at ripening stage 3; BB1: ‘Blanca Bétera’ at ripening stage 1; BB2: ‘Blanca Bétera’ at ripening stage 2; BB3: ‘Blanca Bétera’ at ripening stage 3; BN1: ‘Banane’ at ripening stage 1; BN2: ‘Banane’ at ripening stage 2; BN3: ‘Banane’ at ripening stage 3; TV1: ‘Tres Voltas L’Any’ at ripening stage 1; TV2: ‘Tres Voltas L’Any’ at ripening stage 2; TV3: ‘Tres Voltas L’Any’ at ripening stage 3; BT1: ‘Brown Turkey’ at ripening stage 1; BT2: ‘Brown Turkey’ at ripening stage 2; BT3: ‘Brown Turkey’ at ripening stage 3; SA1: ‘San Antonio’ at ripening stage 1; SA2: ‘San Antonio’ at ripening stage 2; SA3: ‘San Antonio’ at ripening stage 3; DR1: ‘De Rey’ at ripening stage 1; DR2: ‘De Rey’ at ripening stage 2; DR3: ‘De Rey’ at ripening stage 3; CDN1: ‘Cuello Dama Negro’at ripening stage 1; CDN2: ‘Cuello Dama Negro’at ripening stage 2; CDN3: ‘Cuello Dama Negro’at ripening stage 3; CE1: ‘Colar Elche’ at ripening stage 1; CE2: ‘Colar Elche’ at ripening stage 2; CE3: ‘Colar Elche’ at ripening stage 3.

levels, ranging from 1.7 to 2.7 mg per 100 g of FW for skin and from 0.7 to 1 mg per 100 g of FW for flesh. Again, the skin showed a higher content than the flesh. Variety SA showed the highest values of this compound in both tissues. Regarding flavonols, quercetin-3-acetylglucoside and quercetin-3-

brown-, green-, and yellow-green–coloured varieties both in skin and flesh. Veberic et al. (2008) also found that the cultivar ‘Škofjotka’, a white fig type with yellow flesh, showed high amounts of this compound. Another phenolic acid, ellagic acid, appeared in relatively high 209

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Fig. 4. Loading plot and score plot after principal components analysis of the variables and individuals in the plane by two first principal components (PC1 and PC2) in flesh. CDB1: ‘Cuello Dama Blanco’ at ripening stage 1; CDB2: ‘Cuello Dama Blanco’ at ripening stage 2; CDB3: ‘Cuello Dama Blanco’ at ripening stage 3; BB1: ‘Blanca Bétera’ at ripening stage 1; BB2: ‘Blanca Bétera’ at ripening stage 2; BB3: ‘Blanca Bétera’ at ripening stage 3; BN1: ‘Banane’ at ripening stage 1; BN2: ‘Banane’ at ripening stage 2; BN3: ‘Banane’ at ripening stage 3; TV1: ‘Tres Voltas L’Any’ at ripening stage 1; TV2: ‘Tres Voltas L’Any’ at ripening stage 2; TV3: ‘Tres Voltas L’Any’ at ripening stage 3; BT1: ‘Brown Turkey’ at ripening stage 1; BT2: ‘Brown Turkey’ at ripening stage 2; BT3: ‘Brown Turkey’ at ripening stage 3; SA1: ‘San Antonio’ at ripening stage 1; SA2: ‘San Antonio’ at ripening stage 2; SA3: ‘San Antonio’ at ripening stage 3; DR1: ‘De Rey’ at ripening stage 1; DR2: ‘De Rey’ at ripening stage 2; DR3: ‘De Rey’ at ripening stage 3; CDN1: ‘Cuello Dama Negro’at ripening stage 1; CDN2: ‘Cuello Dama Negro’at ripening stage 2; CDN3: ‘Cuello Dama Negro’at ripening stage 3; CE1: ‘Colar Elche’ at ripening stage 1; CE2: ‘Colar Elche’ at ripening stage 2; CE3: ‘Colar Elche’ at ripening stage 3.

reported higher levels in the skin than in the flesh. Quercetin-3-acetylglucoside has only been described by Vallejo et al. (2012) in the skin of fig fruits, however, we identified this compound both in skin and flesh. For skin, the concentration varied between 0.8 to 3.6 mg per 100 g of FW, for flesh, it was in the range of 0.5 to 0.6 mg per 100 g of FW. Among the evaluated phenolic acids and flavonols, we found

O-rutinoside were identified, of which the latter showed a relatively high level. The concentrations of quercetin-3-O-rutinoside varied from 2.9 (BB) to 11.9 (CE) for skin, but ranged from 0.1 (DR) to 1.02 (CE and CDN) mg per 100 g of FW for flesh. Similar results have been reported by Vallejo et al. (2012) and Veberic et al. (2008) who found that this compound was present in the highest concentrations among all the phenolic compounds analysed. Additionally, Vallejo et al. (2012) also 210

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polyphenols and anthocyanins in skin and flesh.

significant differences between varieties and ripening stages (Tables 2 and 3). Generally, highest levels of phenolic acids and flavonols were reached at ripening stage three. A similar tendency has been described by Serradilla et al. (2011) for sweet cherries. As mentioned earlier, proanthocyanins were identified with phloroglucinolysis, and we mainly found monomers of (+)-catechin and (−)-epicatechin, with significant differences between varieties (Table 4). Variety CDN showed the highest levels of (−)-epicatechin, with 16.9 mg per 100 g of FW for skin and 7.2 mg per 100 g of FW for flesh. Conversely, this variety showed the lowest amounts of (+)-catechin, with 4.5 mg per 100 g of FW for skin and 2.0 mg per 100 g of FW for flesh. For (+)-catechin, the cultivar TV had the highest values, with 17.3 mg per 100 g of FW for skin and 5.8 mg per 100 g of FW for flesh. Veberic et al. (2008) found higher values of (+)-catechin than (−)-epicatechin in the studied varieties. Our results show that the relation between (+)-catechin and (−)-epicatechin is strongly influenced by genotype. Additionally, the concentrations measured in our study were higher than those obtained by Veberic et al. (2008) and lower than those reported by Vallejo et al. (2012) for fig flesh. In contrast, we found significant differences between ripening stages, with an increase in (+)-catechin and (−)-epicatechin levels from stage one to stage three (Tables 2 and 3). In general, the studied varieties as well as the different ripening stages were a source of statistically significant variation for all evaluated phenolic compounds. The concentration of anthocyanins depended mainly on the factor ‘variety’, while the factors ‘stage’ and the interaction ‘variety x stage’ did not show significant differences (Tables S1 and S2). On the other hand, the interaction factor ‘variety x stage’ showed a great influence on flavonols and proanthocyanins at the skin level, while at the flesh level, this influence was lower; even the compound quercetin-3-acetylglucoside did not show significant difference. With respect to phenolic acids, the factor interaction ‘variety x stage’ did not show a significant difference both in skin and flesh, depending mainly on the factor ‘genotype’ more than on the factor ‘stage’.

4. Conclusions Several studies have reported high concentrations of bioactive compounds in figs, even higher than those of red wine or tea. The present paper demonstrates, for the first time, that the influence of the ripening stage on bioactive compounds and antioxidant activity in figs is directly related to the genotype. As demonstrated, dark-coloured and brown-coloured varieties were more affected by the influence of ripening than green-, and yellow-green-coloured varieties. In addition, the green-coloured variety BN was also characterised by increased levels of vitamin C, (+)-catechin and L-TAA throughout the ripening process at the flesh level. Nowadays, CDN, CE (also known as ‘Black Mission’) and CDB (also known as ‘Kadota’) are among the mostly consumed fig varieties. Based on our results, it is advisable to increase the consumption of dark figs due to their high amounts of bioactive compounds with antioxidant capacities. In Spain, figs at the commercial ripening stage are typically peeled prior to consumption; however, we advise the consumption of dark-coloured figs with skin and harvested fully ripe. However, further studies would be needed to increase the shelf life of fully ripe figs as well as evaluating the effect of these postharvest treatments on bioactive compounds and their antioxidant activity. Ultimately, the actual bioavailability, as well as the bioactivity of these bioactive compounds identified in figs, also require further investigation. Acknowledgements Financial support for this research was provided by the Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria (INIA), Ministerio de Economía y Competitividad (Spain) (Proyect grant RTA 2010-00123). C. Pereira was financed by an INIA (Grand 30 (BOEn∘31, Sec. III. pág.: 12862)) doctoral fellowship.

3.5. Multivariate analysis

Appendix A. Supplementary data

Principal components analysis (PCA) was performed on all variables studied in both skin and flesh in order to characterise and distinguish each of the nine cultivars and ripening stages. The results presented herein shown that dark-coloured varieties such as CDN, DR and CE as well as the brown-coloured variety SA were characterised by the greatest changes throughout the ripening process compared to the green-, and yellow-green varieties. Dark-coloured and brown-coloured varieties were clearly located on the right-hand side of the bidimensional plot and mainly positively correlated with anthocyanin and TP values (Fig. 3). Therefore, these varieties were more affected by the ripening stage with regards to the composition of bioactive compounds and H-TAA at the skin level. In contrast, green-, and yellow-green-coloured varieties, located on the left-hand side of the bidimensional plot, were not that influenced by the ripening process at the skin level (Fig. 3). Notwithstanding, at the flesh level, again, dark-coloured and brown-coloured varieties were more affected by the ripening stage, clearly showing differences between the stages (Fig. 4). However, in the green-coloured variety BN, ripening had a significant impact on bioactive compounds and antioxidant activity, specially vitamin C, (+)-catechin and L-TAA. On the other hand, at the skin level, contents of total vitamin C and quercetin-3-O-rutinoside were positively correlated with the H-TAA fraction, apart from the anthocyanin concentration, corroborating the importance of these compounds on the antioxidant capacity of these fruits. Conversely, at the flesh level, the H-TAA fraction depended mainly on total phenolic and anthocyanin contents. Finally, L-TAA was mainly related to the concentration of (+)-catechin both in skin and flesh. In previous studies, Solomon et al. (2006) also found a direct relation between the highest antioxidant capacity and the high levels of

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