O R I G I N A L A R T I C L E
The influence of fermentation and bud sizes on antioxidant
activity and bioactive compounds of three different size buds
of Capparis ovata Desf. var. canescens plant
Mehmet Musa O¨ zcan1•Isam A. Mohamed Ahmed2•Fahad Al Juhaimi2• Nurhan Uslu1•Magdi A. Osman2• Mustafa A. Gassem2•Elfadıl E. Babiker2• Kashif Ghafoor2
Revised: 20 December 2019 / Accepted: 20 February 2020 / Published online: 2 March 2020 Ó Association of Food Scientists & Technologists (India) 2020
Abstract The impact of fermentation and bud size on the antioxidant activity, total phenolic content (TPC), and bioactive compounds of caper buds were investigated. The results showed significant differences in the bioactive properties depending on bud sizes and fermentation pro-cess. Antioxidant activity values of fresh caper buds were ranged between 69.61% (bid size) and 72.78% (small size), whereas the values of fermented ones varied between 12.50% (big size) and 39.09% (small size). TPC of fresh caper buds were found in the range of 357.81 mg GAE/ 100 g (medium size) and 372.22 mg GAE/100 g (small size), while those of fermented buds were ranged from 167.53 mg GAE/100 g (medium) to 246.01 mg GAE/ 100 g (small). Apigenin-7-glucoside, (?)-catechin, 1,2-di-hydroxybenzene, and 3,4-dihydroxybenzoic, syringic, and gallic acids were the major phenolic compounds in both fresh and fermented caper buds. Overall, this study clearly demonstrated that both fermentation process and bud size significantly affected the antioxidant activity, TPC, and phenolic compounds of caper buds.
Keywords Antioxidant activity Caper bud size Fermentation Phenolic compounds Total phenolic content
Introduction
Capers (Capparis ovata Desf. var. canescens) is a common aromatic plant that grow wildly in desert areas of the Mediterranean regions (Mattha¨us and O¨ zcan 2005; Tesoriere et al.2007). In these regions, the major producers of capers are Spain, Italy, Tunisia, Turkey, and Morocco (Inocencio et al.2002; Mattha¨us and O¨ zcan 2005; Romeo et al. 2007; Tlili et al. 2010) where the fruits and flower buds of Capparis spp are processed and then used for human consumption (Francesca et al. 2016). The recent decades are witnessed by a significant increase in the interest of bioactive compounds form plant products (Zhang and Ma 2018; El-Waseif and Badr 2018). Polyphenols are one of the major groups of plant-derived bioactive compounds which are commonly found in many plant-based foods constituents like cereals, vegetables, fruits, chocolate and beverages. As the secondary metabolites in plants, phenolic compounds play a critical roles in the defense system against oxidative stresses through different physiological and biochemical mecha-nisms (Goldberg et al. 2003; Shahidi and Naczk 2004; Stevenson and Hurst 2007; Weichselbaum and Buttriss 2010; Tlili et al. 2015). Previously, the flower buds of capers have been studied for their antioxidant activity and found to display high antioxidant activity (Germano` et al. 2002). Being the main group of bioactive antioxidants, more attention is directed toward plant polyphenols for preventing and curing human health (Meot-Duros and Magne 2009). The plant polyphenols consist of various important phytochemicals such as phenolic compounds in different parts such as fruits, leaves, roots, stems, buds, bark and seeds (Chedraoui et al. 2017). Consequently, these plants parts were commonly used in folk medicine in the treatment of many illnesses such as toothache, kidney & Mehmet Musa O¨zcan
[email protected] & Isam A. Mohamed Ahmed
1 Department of Food Engineering, Faculty of Agriculture,
Selcuk University, 42031 Konya, Turkey
2 Department of Food Science and Nutrition, College of Food
and Agricultural Sciences, King Saud University, Riyadh, Saudi Arabia
failure, and headache (Tlili et al. 2011; Kalantari et al. 2018). Thus, cultivation and utilization of plants as sources of bioactive antioxidant could have high economic values (Chedraoui et al. 2017). In traditional medicine in many countries, capers are used for preventing and curing numerous diseases due to their antioxidant, antimicrobial, anticancer, antirheumatic, tonic, astringent and diuretic potentials (Rivera et al.2003). In food applications, capers are normally pickled and used as condiment in the prepa-ration of salads (Jime´nez-Lo´pez et al. 2018). In many Mediterranean countries, caper flower buds are commonly commercialized due to their potential applications in foods as condiments or ingredients as they have good and pun-gent flavor (Arpun-gentieri et al.2012). Studies on the bioactive properties of caper flower buds with different sizes as influenced by fermentation process are scarce. Thus, main objective of the present study was to examine the impact of fermentation and bud sizes on antioxidant activity and bioactive phenolics of three different size buds of Capparis ovata Desf. var. canescens plant obtained from Konya province in Turkey.
Material and method
Material
The flower buds of caper (Capparis ovata Desf. var. canescens) were obtained from Konya province, Turkey in June 2019. Different size capers (small (\ 8 mm), 8 mm \ medium \ 13 mm and big ([ 13 mm)) were used for analysis.
Methods
Fermentation process
For fermentation process, the fermentation jars were filled with caper flower buds up to the two-third level. After that, a brine solution (10% salt) was added to fill the remaining part of jars. Caper flower buds were left for fermentation for 45 days at room temperature. At the end of fermenta-tion period, the fermented and unfermented samples of different bud sizes were subjected to analysis for their total polyphenols, antioxidant activity, and phenolic compounds.
Sample extraction
The method of Tlili et al. (2017) was used for extraction of polyphenols from caper samples (fresh and fermented) with slight alterations. Briefly, 1 g of powdered samples of fresh
and fermented buds with different sizes was mixed with 10 mL methanol. The mixture was incubated in the water bath for 3 days. After that, the mixture was filtered using a Whatman No.1 filter paper to remove solid particles. After evaporation of the methanol phase at 50°C, the dried extracts were collected and then melted in 25 mL methanol.
Total phenolic content (TPC)
The colorimetric method using Folin–Ciocalteu (FC) solution was carried out to assess the TPC of caper extracts as described previously (Yoo et al. 2004) with slight modifications. Briefly, 1 mL of the extracts was mixed with 1 mL of Folin-Ciocalteu and kept at room temperature for 5 min. After that, 10 mL of Na2CO3solution was added to the mixture, mixed well, and the volume was made to 25 mL with deionized water. The mixture was incubated at room temperature for 1 h and then the optical density of was measured at spectrophotometrically at 750 nm. Gallic acid was used as authentic standard and treated in the same way of the extracts and used to generate the standard curve. Results were presented as gallic acid equivalent (GAE) per 100 g fresh weight (GAE/100 g FW).
Antioxidant activity
DPPH (1,1-diphenyl-2-picrylhydrazyl) radical scavenging activity of the caper extracts of fresh and fermented caper samples was assessed as shown previously (Lee et al. 1998). In brief, DPPH was dissolved in methanol and then 2 mL of this solution was thoroughly mixed with I mL of caper extracts. After 30 min standing at room temperature, the optical density of the extract and blank was spec-trophotometrically measured at 517 nm to calculate the DPPH inhibition percentage.
Determination of phenolic compounds
Phenolic compounds of fresh and fermented caper samples was determined using high performance liquid chro-matography with Inertsil ODS-3 column (5 lm; 4.6 9 250 mm) fitted to a Shimadzu-HPLC system (Shi-madzu, Kyoto, Japan) with a PDA detector. The mobile phase used to discrete and quantify the phenolic com-pounds of the caper samples was composed of a mixture of A (0.05% Acetic acid in water) and B (acetonitrile) solu-tions. Step gradient program of 8% B (0–0.10 min), 10% B (0.10–2 min), 30% B (2–27 min), 56% B (27–37 min), 8% B (37–37.10 min), and 8% B (37.10–45 min) was applied at a flow rate of 1 mL/min at 30°C. Twenty milliliter of the sample was injected to the column and phenolic com-pounds peaks were detected at 280 and 330 nm. Authentic
standard of phenolic compounds was run on the same conditions and used to identify the peaks in the samples. Statistical analyses
Triplicate treatments and measurements were carried out of caper samples. The experimental design used was a com-pletely randomized design. The data of three determina-tions of TPC, antioxidant activity, and phenolic compounds was statistically analyzed using one-way ANOVA (JMP version 9.0, SAS Inst. Inc., Cary, NC, USA). The results were presented as mean ± standard deviation (MSTAT C) of caper bud samples and fermentation process (Pu¨sku¨lcu¨ and I˙kiz1989). Multivariate analysis was carried out using MULTBIPLOT software as described previously (Vicente-Villardon2010).
Results and discussion
The antioxidant activity and TPC of fresh and fermented caper buds at three different sizes are depicted in Table1. Antioxidant activity of fresh caper buds were changed between 69.61% (big size) and 72.78% (small size), whereas, that of fermented caper buds varied between 12.50% (big size) and 39.09% (small size). Apparently, both bud size and fermentation process affected the antioxidant activity of caper. In addition, TPC of fresh caper buds were found between 357.81 mg GAE/100 g (medium size) and 372.22 mg GAE/100 g (small size), while total phenol contents of fermented caper buds were ranged from 167.53 mg GAE/100 g (medium size) to 246.01 mg GAE/100 g (small size). Noticeably the results exhibited variances depending on bud sizes and fermenta-tion process. Antioxidant activity of fermented caper buds decreased compared to results of fresh caper buds. Also, antioxidant activity of caper buds decreased as the bud size increased. TPC of both fresh and fermented medium and big caper buds were lower than those of small size buds.
However, TPC of both fresh and fermented medium size buds were seen partially lower than those of big size buds. In general, antioxidant activity and TPC of both fresh and fermented small caper buds were higher compared to the two other buds (medium and big). The significant decrease in antioxidant activity and TPC of fermented buds com-pared to fresh buds could possibly be due to the activity of fermenting microorganisms and enzymes naturally found in the bud structure during fermentation. Grimalt et al. (2018) stated that total antioxidant activity of caper fruits changed between 24.0 mg Trolox/100 g (thin fruit) and 102.6 mg Trolox/100 g (thick fruit) for OKI 4 cultivar. In addition, the same authors reported a range of 61.5 and 119.2 mg GAE/100 g for TPC in ALB2 caper fruit cultivar (Grimalt et al. 2018). The findings of the current study demonstrated that TPC of caper buds were greater com-pared to those reported previously by Fu et al. (2011) in many fruits such mango (3.037 mg GAE/100 g), apple (58.12 mg GAE/100 g) and avocado (21.86 mg GAE/ 100 g). In addition, another report showed that TPC and antioxidant activity of caper bud (C. spinosa) were 48.75 mg GAE/100 g and 2.37 Trolox equivalents/g, respectively (Tesoriere et al.2007). Moreover, while TPC of caper fruit cultivars was found in the range of 6.5 and 11.1 mg GAE/g, antioxidant activity values of caper fruits found between 0.98 g Trolox equivalent/100 g and 1.48 g Trolox equivalent/100 g (Jime´nez-Lo´pez et al. 2018). Furthermore, it has been stated that TPC and rutin values of caper flower buds obtained from different areas in Tunisia were found between 1.903 and 3.870 mg GAE/100 g to 34.4 and 1070.7 mg/100 g, respectively (Tlili et al.2010). The phenolic compounds of fresh and fermented caper buds at three different sizes are given in Table2. The results indicated that (?)-catechin, 1,2-dihydroxybenzene, apigenin-7-glucoside, and gallic, 3,4-dihydroxybenzoic, and syringic acids were the major bioactive compounds of both fresh and fermented caper buds. The quantities of individual phenolic compounds were differed significantly between the bud sizes. In fresh caper buds, the highest Table 1 Antioxidant activity
and total phenolic content of capers
Size of caper Antioxidant activity (%) Total phenolic content (mgGAE/100 g) Fresh
Caper (small) 72.78 ± 0.01*a 372.22 ± 0.07 a Caper (medium) 71.07 ± 0.01b** 357.81 ± 0.02 c Caper (big) 69.61 ± 0.01c 361.28 ± 0.03 b Fermented Caper (small) 39.09 ± 0.02 a 246.01 ± 0.04 a Caper (medium) 20.56 ± 0.00 b 167.53 ± 0.04 c Caper (big) 12.50 ± 0.00 c 190.45 ± 0.08 b *mean ± standard deviation
values of gallic acid, 3,4-dihydroxybenzoic acid, (?)-cat-echin and kaempferol were observed in small size buds, whereas, the least values of these phenolics were observed in big size buds except 3,4-dihydroxybenzoic acid which is low in medium size buds. In addition, 1,2-dihydroxyben-zene, rutin-trihydrate, resveratrol, and isorhamnetin were high in medium size buds, while the reset of phenolic compounds were high in big size buds. In fermented buds, the highest values of gallic acid, (?)-catechin, syringic acid, naringenin, and kaempferol were found in small size buds. The highest values of all other phenolic compounds were recorded in big size buds. With view exceptions, both fresh and fermented buds of small and big sizes contain greater quantities of most phenolic compounds compared to medium size buds. These findings suggested that the size of the buds significantly affected to the phenolic compo-sition of caper. The variation in quantities of phenolic compounds between different bud sizes could be attributed to the maturity stage of the buds in which formation and decomposition of phenolic compounds are occurred due to indigenous enzymes. Fermentation of caper buds showed varied effects on the phenolic compounds. It reduced the amounts of the phenolic acids (gallic, 3,4-dihydroxyben-zoic, caffeic acids), (?)-catechin, rutin trihydrate, and resveratrol in all buds, p-coumaric and trans-ferulic acids in medium size buds, syringic acid in big size buds, api-genin- 7-glucoside in small buds, and quercetin in small
and medium size buds. However, this treatment increased the values of 1,2-dihydroxybenzene, trans-cinnamic acid, naringenin, kaempferol, and isorhamnetin in all buds, syringic acid in small and medium size buds, and p-cou-maric acid, trans-ferulic acid, apigenin-7-glucoside and quercetin in big size buds. It is thought that the decrease in the phenolic component contents of fermented caper buds is generally caused by microorganism and enzyme activity in the structure of the bud during fermentation as well as harvest time, maturity and climatic factors. Most of the phenolic components of both fresh and fermented caper buds decreased with increasing bud size. The high con-centration of certain compounds such as 1,2-dihydroxy-benzene, syringic acid, naringenin, kaempferol and isorhamnetin of fermented caper buds compared to fresh caper results may be due to metabolites and color pigments formed by microorganisms during fermentation. It is well known that human consumption of fruits and vegeta-bles rich diets is recommended as the phenolic compounds in these diets could inhibit the mutagenesis and carcino-genesis in human cells (Weisburger1992). In this regard, rich phenolic profile of caper buds could make these buds as potential source of phenolic compounds if they con-sumed regularly in both fresh and fermented forms. Caper bud extract contained 0.16 g/100 g rutin (Tesoriere et al. 2007). Francesca et al. (2016) determined 1.04 lg/g epi-catechin, 21.08 lg/g rutin, 1.20 lg/g myrcetin in caper Table 2 Phenolic compounds of fresh and fermented capers
(mg/100 g) Fresh caper buds Fermented caper buds
Small Medium Big Small Medium Big
Gallic acid 78.30 ± 1.68*a 69.12 ± 1.23b 64.57 ± 0.65c 43.14 ± 0.14a 36.26 ± 1.88b 34.42 ± 0.90c 3,4-Dihydroxybenzoic acid 125.84 ± 4.73a** 112.08 ± 1.42c 115.31 ± 2.51b 26.46 ± 2.40b 13.96 ± 1.94c 50.40 ± 0.62a (?)-Catechin 177.80 ± 9.77a 118.62 ± 4.17b 80.21 ± 0.54c 89.24 ± 1.71a 12.85 ± 1.32c 65.50 ± 0.51b 1,2-Dihydroxybenzene 119.68 ± 9.12b 123.32 ± 3.05a 96.68 ± 1.00c 188.89 ± 11.81 183.05 ± 3.58 174.24 ± 0.53 Syringic acid 33.99 ± 3.32c 44.99 ± 0.55b 59.06 ± 0.41a 116.99 ± 5.04a 85.78 ± 0.97b 25.12 ± 0.83c Caffeic acid 30.72 ± 1.83b 22.72 ± 0.39c 31.52 ± 1.07a 15.14 ± 1.47b 1.01 ± 0.15c 19.53 ± 0.62a Rutin-trihydrate 145.18 ± 4.81b 154.47 ± 2.28a 55.25 ± 9.50c 6.86 ± 0.54b 1.02 ± 0.08c 12.54 ± 0.82a p-Coumaric acid 1.15 ± 0.10c 1.58 ± 0.07b 1.66 ± 0.03a 2.74 ± 0.27b 0.59 ± 0.01c 3.91 ± 0.25a trans-Ferulic acid 8.08 ± 0.71c 12.23 ± 0.94b 17.34 ± 0.61a 19.8 ± 1.62b 4.44 ± 0.21c 28.39 ± 0.21a Apigenin 7 glucoside 13.75 ± 1.21b 13.19 ± 1.19c 15.53 ± 0.12a 12.45 ± 0.72c 22.05 ± 1.70b 26.13 ± 0.10a Resveratrol 13.31 ± 0.92c 18.13 ± 1.06a 13.53 ± 0.45b 2.53 ± 0.33b 2.62 ± 0.28b 5.57 ± 0.45a Quercetin 7.25 ± 0.57c 9.23 ± 0.75b 21.30 ± 0.44a 5.11 ± 0.32b 4.16 ± 0.59c 24.97 ± 1.58a trans-Cinnamic acid 1.21 ± 0.05b 1.09 ± 0.02c 2.04 ± 0.02a 1.61 ± 0.22b 1.31 ± 0.09c 2.24 ± 0.12a Naringenin 2.30c ± 0.07 2.98 ± 0.18b 4.68 ± 0.04a 6.88 ± 0.71a 3.48 ± 0.27c 4.79 ± 0.01b Kaempferol 4.34 ± 0.04a 3.70 ± 0.05b 3.46 ± 0.20c 8.07 ± 0.74a 3.64 ± 0.00c 4.08 ± 0.36b Isorhamnetin 1.84 ± 0.10c 3.76 ± 0.26a 3.34 ± 0.08b 6.24 ± 0.48a 6.17 ± 0.37a 4.30 ± 0.40b *mean ± SD
fruit. Caper fruit extracts contained 0.25–0.33 mg/g epi-catechin dimer, 0.4–0.98 mg/g epiepi-catechin, 0.28–0.40 mg/ g epicatechin trimer, 0.054–0.09 mg/g quercetin, 0.093–0.22 mg/g rutin, 0.05–0.07 mg/g kaempferol-o-rutinoside (Jime´nez-Lo´pez et al. 2018). Interestingly, the observed variations in phenolic profile of fermented and unfermented caper buds of different sizes indicated that the fermentation process as well as ripening stages of the buds caused changes in the bioactivity of the buds (Francesca et al. 2016). In agreements with our findings, previous studies on capers demonstrated the presence of quercetin and rutin in the caper fruits (Conforti et al.2011; Khalidi et al.2010). Hydrolysis of rutin by hesperidinase is known as one of the process that could lead to the formation of quercetin (Tranchimand et al.2010).
Correlation analysis between the antioxidant activity, TPC, and phenolic compounds indicated several positive and negative relationships (Table3). Extreme positive association (r2= 0.984) was noted between TPC and antioxidant activity (P \ 0.0001) indicating strong contri-bution of TPC to the antioxidant capacity of caper buds. Among bioactive compounds, gallic acid showed strong positive association (r2= 0.967, P \ 0.001) with antioxi-dant activity in addition to 3,4-dihydroxybenoic (r2= 0.885, P\ 0.05), rutin-trihydrate (r2= 0.833, P\ 0.05) and resveratrol (r2= 0.861, P \ 0.05) signifying the impact of these bioactive compounds on the antioxidant capacity of caper buds. However, the negative (P \ 0.05) correlation of 1,2-dihydroxybenzene (r2= - 0.872) and apigenin-7- glucoside (r2= - 0.816) with antioxidant activity indicated negative impacts of these phenolic compounds on the DPPH radical scavenging activity of caper buds. Positive correlation of TPC with gallic acid (r2= 0.969, P\ 0.001), 3,4-dihydroxybenzoic acid (r2= 0.940, P \ 0.01), caffeic acid (r2= 0.854, P \ 0.05), rutin-trihydrate (r2= 0.843, P \ 0.05), and resveratrol (r2= 0.891, P \ 0.01) was evident, whereas, it correlated negatively with 1,2-dihydroxybenzene (r2= - 0.905, P\ 0.01) signifying the impact of these phenolic pounds on the TPC of caper buds. Among phenolic com-pounds, 1,2-dihydroxybenzene and isorhamnetin negatively correlated with gallic and 3,4-dihydroxybenzoic acids. Gallic acid exhibited positive correlations with 3,4-dihydroxybenzoic acid (r2= 0.932, P \ 0.01), (?)-cate-chin (r2= 0.839, P \ 0.05), rutin-trihydrate (r2= 0.913, P\ 0.01), and resveratrol (r2= 0.880, P\ 0.05). Whereas, 3,4-dihydroxybenzoic acids positively associated with caffeic acid (r2= 0.899, P \ 0.01), rutin tryhydrate (r2= 0.862, P\ 0.05), and resveratrol (r2= 0.939, P\ 0.01). Positive correlations were observed between (?)-catechin and rutin tryhydrate (r2= 0.825, P \ 0.05), 1,2-dihydroxybenzene and isorhamnetin (r2= 0.832, P\ 0.05), rutin trihydrate and resveratrol (r2= 0.902,
P\ 0.01), p-coumaric acid and trans-ferulic acid (r2= 0.970, P \ 0.001), trans-ferulic and trans-cinnamic acids (r2= 0.829, P \ 0.05), and quercetin and trans-cin-namic acid (r2= 0.859, P \ 0.05). Whereas, negative correlations were existed between caffeic acid and isorhamnetin (r2= - 0.870, P \ 0.05), and 1,2-dihydrox-ybenzene with caffeic acid (r2= - 0.832, P \ 0.05) and resveratrol (r2= - 0.901, P \ 0.01) indicating the influ-ence of these compounds on each other in caper buds. Generally, the findings of this study demonstrated that all detected phenolic compounds did not involve in the antioxidant activity of caper buds.
The interrelationship between treatments (fresh, fer-mented, and bud size) and antioxidant activity, TPC and phenolic compounds was profoundly determined using HJ-Biplot analysis. In the biplot, the distance between treat-ments indicated the relationship between them in their bioactive properties in which short distance indicates similarity while long distance indicates dissimilarity. The cosine of angles between the vectors indicates correlations, where, positive correlations is appeared as acute (\ 90°) angles, negative correlations as obtuse ([ 90°) or strait angles (180°), and no correlation as right (90°) angle (Yan and Fregeau-Reid 2008). The results clearly showed an exceptional input of the principle components axes (PC1 and PC2) to the entire variability (78.72%) of the blotted data (Fig. 1). Interestingly, the treatments (fermented and unfermented) were distinctly grouped according to their effects on the specific bioactive properties of different sizes of caper buds. Regardless of the bud size, the group cluster in the right of the graph contained the fermented caper buds, whereas, that in the left side of the graph represent the fresh ones. The cluster of fresh buds was characterized by high values of antioxidant activity, TPC, gallic acid, rutin-trihydrate, (?)-catechin, resveratrol, 3,4-dihydroxy-benzoic acid, and caffeic acid. The acute cosine of the angles between these traits indicated positive correlations among them. Whereas, the cluster of fermented buds is characterized by higher values of syringic acid, kaemp-ferol, isorhamnetin, 1,2-dihydroxybenzene, naringenin, apigenin-7-glucoside, p-coumaric acid, trans-ferulic acid, trans-cinnamic acid, and quercetin. Regarding the bud size, the small and medium size buds are very close to each other in the bioactive properties compared to big size buds. Interestingly, the findings of this study clearly demon-strated that both fermentation and bud size significantly affected the antioxidant activity, TPC, and phenolic com-pounds of caper buds.
Table 3 Correlation coefficients of antioxidant activity, total phenolic, phenolic compounds of different size buds of Capparis ovata Desf. var. canescens Antioxidant TPC Gallic 3,4- Dihydroxybenzoic (? )-Catechin 1,2- Dihydroxybenzene Caffeic Rutin trihydrate p -Coumaric trans -Ferulic Quercetin TPC 0.984**** Gallic 0.967*** 0.969*** 3,4- Dihydroxybenzoic 0.885* 0.940** 0.932** (? )-Catechin 0.839* 1,2- Dihydroxybenzene -0.872* -0.905** -0.872* -0.950*** Caffeic 0.854* 0.899** -0.832* Rutin trihydrate 0.833* 0.843* 0.913** 0.862* 0.825* Trans-Ferulic 0.970*** Apigenin 7 glucoside -0.816* Resveratrol 0.861* 0.891** 0.880* 0.939** -0.901** 0.902** Trans-Cinnamic 0.829* 0.859* Isorhamnetin -0.831* -0.929** 0.832* -0.870* * P \ 0.05 ** P \ 0.01 *** P \ 0.001 **** P \ 0.0001
Conclusion
The small size buds of fresh and fermented caper showed the highest phenolic content a combined with best antiox-idant activity through all samples. In addition, the small size buds of fresh and fermented caper also exhibited a good antioxidant activity. The phenolic profile of caper buds showed variation in phenolic compounds depending on size of buds and fermentation treatment. The findings of the present study propose that both fresh and fermented caper buds may be used as a possible source of natural antioxidant for various applications in food and medicine. However, care about the bud size should be taken during the application of caper buds as antioxidant source as it greatly affected the bioactive properties of caper buds with high preference to the small size buds.
Acknowledgements The authors would like to extend their sincere appreciation to the Deanship of Scientific Research at King Saud University for its funding the Research group no (RG-1439-080). Technical support of RSSU at King Saud University is also well appreciated.
References
Argentieri M, Macchia F, Papadia P, Fanizzi FP, Avato P (2012) Bioactive compounds from Capparis spinosa subsp. rupestris. Ind Crops Prod 36:65–69
Chedraoui S, Abi-Rizk A, El-Beyrouthy M, Chalak L, Ouaini N, Raijou L (2017) Capparis spinosa L. in a systematic review: a xerophilous species of multi values and promising potentialities for agrosystems under the threat of global warming. Front Plant Sci 8:1845
Conforti F, Marcotullio MC, Menichini F, Statti GA, Vannutelli L, Burini G, Menichini F, Curini M (2011) The influence of collection zone on glucosinolates, polyphenols and flavonoid-scontents and biological profiles of Capparis sicula ssp. sicula. Food Sci Technol Int 12(2):87–97
El-Waseif MA, Badr SA (2018) Using Egyptian caper seed oil (Capparis spinosa L.) as a natural antioxidant to improving oxidative stability of frying oils during fat frying. World J Dairy Food Sci 13(1):18–30
Francesca N, Barbera M, Martorana A, Saiano F, Gaglio R, Aponte M, Moschetti G, Settanni L (2016) Optimised method for the analysis of phenolic compounds from caper (Capparis spinosa L.) berries and monitoring of their changes during fermentation. Food Chem 196:1172–1179
Fu L, Xu BT, Xu XR, Gan RY, Zhang Y, Xia EQ, Li HB (2011) Antioxidant capacities and total phenolic contents of 62 fruits. Food Chem 129:345–350
Germano` MP, De Pasquale R, D’Angelo V, Catania S, Silvari V, Costa C (2002) Evaluation of extracts and isolated fraction from Capparis spinosa L. buds as an antioxidant source. J Agric Food Chem 50:1168–1171
Fig. 1 The HJ-biplot based on principal component analysis for bioactive properties of different sizes of fresh and fermented caper flower buds
Goldberg DM, Yan J, Soleas GJ (2003) Absorption of three wine-related polyphenols in three different matrices by health subjects. Clin Biochem 36(1):79–87
Grimalt M, Herna´ndez F, Legua P, Almansa MS, Amoro´s A (2018) Physicochemical composition and antioxidant activity of three Spanish caper (Capparis spinosa L.) fruit cultivars in three stages of development. Sci Hort 240:509–515
Inocencio C, Alcaraz F, Calderon F, Obon C, Rivera D (2002) The use of floral characters in Capparissect. Capparisto determine the botanical and geographical origin of capers. Eur Food Res Technol 214:335–339
Jime´nez-Lo´pez J, Ruiz-Medina A, Ortega-Barrales P, Llorent-Martı´nez EJ (2018) Phytochemical profile and antioxidant activity of caper berries (Capparis spinosa L.): evaluation of the influence of the fermentation process. Food Chem 250:54–59 Kalantari H, Foruozandeh H, Khodayar MJ, Siahpoosh A, Saki N, Kheradmand P (2018) Antioxidant and hepatoprotective effects of Capparis spinosa L. fractions and Quercetin on tert-butyl hydroperoxide- induced acute liver damage in mice. J Trad Complement Med 8:120–127
Khalidi A, Triki S, Munne-Bosch S (2010) Phenolic compounds and vitamin antioxidants of Caper (Capparis spinosa). Plant Foods Hum Nutr 65:260–265
Lee SK, Mbwambo ZH, Chung HS, Luyengi L, Games EJC, Mehta RG (1998) Evaluation of the antioxidant potential of natural products. Comb Chem High Throughput Screen 1:35–46 Mattha¨us B, O¨ zcan M (2005) Glucosinolates and fatty acid, sterol and
tocopherol composition of seed oils from Capparis spinosa var. spinosa and Capparis ovata Desf. var. canescens (Coss.) Heywood. J Agric Food Chem 53:7136–7141
Meot-Duros L, Magne C (2009) Antioxidant activity and phenol content of Crithmum maritimum L. leaves. Plant Physiol Biochem 47:37–41
Pu¨sku¨lcu¨ H, Ikiz F (1989) Introdiction to statistic. Bilgehan Press, Izmir, p 333 (in Turkish)
Rivera D, Inocencio C, Obo´n MC, Alcaraz F (2003) Review of food and medicinal uses of Capparis L. subgenus Capparis (Cap-paridaceae). Econ Bot 57:515–534
Romeo V, Ziino M, Giuffrida D, Condurso C, Verzera A (2007) Flavour profile of capers (Capparis spinosa L.) from the Eolian archipelago by HS-SPME/GC-MS. Food Chem 101:1272–1278 Shahidi F, Naczk M (2004) Phenolic in food and nutraceutical. CRC
Press, Boca Raton, pp 1–558
Stevenson DE, Hurst RD (2007) Polyphenolic phytochemicals-just antioxidants or much more? Cell Mol Life Sci 64:2900–2916
Tesoriere L, Bufera D, Gentile C, Livrea MA (2007) Bioactive components of caper (Capparis spinosa L.) from Sicily and antioxidant effects in a red meat simulated gastric digestion. J Agric Food Chem 55:8465–8471
Tlili N, Khaldi A, Triki S, Munne-Bosch S (2010) Phenolic compounds and vitamin antioxidants of caper (Capparis spinosa). Plant Food Hum Nutr 65:260–265
Tlili N, Nasri N, Khaldi A, Triki S, Munne´-Bosch S (2011) Phenolic compounds, tocopherols, carotenoids and vitamin C of commer-cial caper. J Food Biochem 35:472–483
Tlili N, Mejri H, Anouer F, Saadaoui E, Khjaldi A, Nasri N (2015) Phenolic profile and antioxidant activity of Capparis spinosa seeds harvested from different wild habitats. Ind Crops Prod 76:930–935
Tlili N, Feriani A, Saadoui E, Nasri N, Khaldi A (2017) Capparis spinosa leaves extract: source of bioantioxidants with nephro-protective and hepatoprotective effects. Biomed Pharm 87:171–179
Tranchimand S, Brouant P, Iacazio G (2010) The rutin catabolic pathway with special emphasis on quercetinase. Biodegradation 21:833–859
Vicente-Villardon JL (2010) MULTBIPLOT: a package for multi-variate analysis using biplots. Department of Statistics, Univer-sity of Salamanca, Salamanca
Weichselbaum E, Buttriss JL (2010) Polyphenols in the diet. Nutr Bull 35(2):157–164
Weisburger JH (1992) Mutagenic, carcinogenic, and chemopreven-tive effects of phenols and catechols. The underlying mecha-nisms. In: Huang M-T, Ho C-T, Lee CY (eds) Phenolic compounds in food and their effects on health II. Antioxidants and cancer prevention. American Chemical Society, New Jersey, pp 35–47
Yan W, Fregeau-Reid J (2008) Breeding line selection based on multiple traits. Crop Sci 48(2):417–423
Yoo KM, Lee KW, Park JB, Lee HJ, Hwang IK (2004) Variation in major antioxidants and total antioxidant activity of Yuzu (Citrus junos SiebexTanaka) during maturation and between cultivars. J Agric Food Chem 52:5907–5913
Zhang H, Ma ZF (2018) Phytochemical and pharmacological properties of Capparis spinosa as a medicinal plant. Nutrients 10:2–14
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