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Page 1 of 38 Food & Function Food & Function Accepted Manuscript This is an Accepted Manuscript, which has been through the Royal Society of Chemistry peer review process and has been accepted for publication. Accepted Manuscripts are published online shortly after acceptance, before technical editing, formatting and proof reading. Using this free service, authors can make their results available to the community, in citable form, before we publish the edited article. We will replace this Accepted Manuscript with the edited and formatted Advance Article as soon as it is available. You can find more information about Accepted Manuscripts in the Information for Authors. Please note that technical editing may introduce minor changes to the text and/or graphics, which may alter content. The journal’s standard Terms & Conditions and the Ethical guidelines still apply. In no event shall the Royal Society of Chemistry be held responsible for any errors or omissions in this Accepted Manuscript or any consequences arising from the use of any information it contains. www.rsc.org/foodfunction Page 1 of 38 Food & Function 1 Assessment of the distribution of phenolic compounds and contribution to the 2 antioxidant activity in Tunisian figs leaves, fruits, skins and pulps using mass 3 spectrometry-based analysis. 4 5 Sonda Ammar, a,b María del Mar Contreras, a,c, * Olfa Belguith-Hadrich, b Antonio Segura- 6 Carretero,a,c Mohamed Bouaziz b* 7 aResearch and Development Functional Food Centre (CIDAF), Bioregión Building, Health 8 Science Technological Park, Avenida del Conocimiento 37, 18016, Granada, Spain. 9 bLaboratoire d’Électrochimie et Environnement, École Nationale d’Ingénieurs de Sfax BP 10 “1173” 3038, Université de Sfax, Tunisia. Manuscript 11 cDepartment of Analytical Chemistry, Faculty of Sciences, University of Granada. Avda. 12 Fuentenueva s/n, 18071 Granada, Spain. 13 14 *Corresponding authors: Accepted 15 M. d. M. Contreras at Department of Analytical Chemistry, University of Granada. Avda. 16 Fuentenueva s/n, 18071 Granada, Spain. Tel.: +34 958 637 206; fax: +34 958 637 083; E-mail 17 address: [email protected] or [email protected] 18 M. Bouaziz at Laboratoire d’Électrochimie et Environnement, École Nationale d’Ingénieurs Function 19 de Sfax BP “1173” 3038, Université de Sfax, Tunisia. Tel.: +216 98 667 581; fax: +216 74 & 20 674 364 E-mail address: [email protected] . 21 22 Food 23 24 25 1 Food & Function Page 2 of 38 26 Abstract 27 The phenolic composition of leaves, fruits, skins and pulps from two F. carica cultivars, 28 ‘Temri’ and ‘Soltani’, was studied in order to understand its contribution to the antioxidant 29 activity. A total of 116 compounds were characterized based on the results obtained by 30 reversed-phase ultra-high performance liquid chromatography coupled to diode array and 31 mass spectrometry detection. In general, the leaves of both cultivars and the skin of ‘Soltani’ 32 presented richer qualitative profiles compared to the other plant parts. Using the negative 33 ionization mode, qualitative profiles of the same part of the studied figs were similar. In this 34 regard, rutin was the main compound in fruits, skins and leaves, but with different relative Manuscript 35 amounts. Alternatively, an isomer of prenylhydroxygenistein was the maJor compound in the 36 pulps. In the positive ionization mode, 9 anthocyanins were characterized in ‘Soltani’ skin, 37 only two of them being also present in the green cultivar ‘Temri’. The main anthocyanins 38 were cyanidin 3-rutinoside and cyanidin 3,5-diglucoside, depending on the cultivar and fruit 39 part. In this ionization mode, 14 furanocoumarins were also detected in the leaves of both Accepted 40 studied cultivars with methoxypsoralen and psoralen being the most relatively abundant. In 41 addition, our findings showed a good correlation between the antioxidant activity, total phenol 42 content, and abundance of some phenolic subfamilies such as hydroxybenzoic acids, 43 flavonols, flavones, hydroxycoumarins and furanocoumarins with r > 0.97. Function 44 & 45 Keywords: 46 Anthocyanins; antioxidant activity; Ficus carica ; furanocoumarins; Moraceae; RP-UHPLC- Food 47 DAD-QTOF-MS; phenolic compounds. 48 2 Page 3 of 38 Food & Function 49 Introduction 50 Moraceae is a family with widespread distribution in the tropics and subtropics, but it 51 also occurs in temperate regions.1 This family includes well-known plants such as figs, 52 banyans, breadfruits, mulberries, and osage-oranges.2 Ficus constitutes one of the thirty-seven 53 geniuses of this family, with about 800 species. 3 Among them, F. carica (fig tree or common 54 fig) is one of the oldest known fruits crop, which is used for fruit production.4 Alongside the 55 olive trees, F. carica is considered a biomarker of the Mediterranean ecosystem, its fig fruits 56 are also consumed fresh, dried, preserved, canned, and candied.5 57 Phenolic compounds are secondary metabolites biosynthesized by plants both during Manuscript 58 normal development and in response to stress conditions.6 Polyphenols significantly 59 contribute to the organoleptic properties of fruits: colour, bitterness and astringency. 7 60 Furthermore, these minor compounds could be beneficial for human health.8 Several 61 researches on F. carica have shown changes in the figs phenolic composition as a 8,9 5,10,11 4 62 consequence of the cultivar, drying or extraction method, pollinization, sampling date Accepted 63 and maturation.5,12 Other studies have focused on particular phenolic classes, such as 64 anthocyanins in fig fruits 9,13 and furanocoumarins in leaves. 10 Interestingly, F. carica exhibits 65 antiplatelet, antispasmodic and anti-inflamatory activity, 14 but little is known about their 66 active compounds and qualitative and quantitative differences in F. carica plant parts. In this Function 67 regard, some authors have attributed these beneficial properties to the presence of phenolic & 68 compounds, although it has not been demonstrated in depth.9,13 69 Conventionally, the phenolic content is evaluated through colorimetric methods. Food 70 However, these studies should be complemented with more specific and selective analytical 71 methodologies in order to fully understand the relationship between the phenolic composition 72 and health.15 In addition, these novel analytical techniques may be useful in order to identify 73 new sources of phenolic compounds that are underused or usually disposed of as waste 3 Food & Function Page 4 of 38 74 material in many food processing industries, such as leaves or fruit peels.16 The analytical 75 techniques used to study F. carica includes gas chromatography coupled to mass 76 spectrometry (MS) and a flame ionization detector (FID), 12 as well as liquid chromatography 77 (LC) coupled to UV/Vis or diode array detection (DAD) and mass spectrometry (MS) in a 78 negative or positive ionization mode depending on the target phenolic class. 10,11,13,17–19 As 79 commented above, the composition of phenolic compounds is not only influenced by the 80 cultivar, but also varies depending on the part studied.18 In this context, Solomon et al. 9 81 described differences in total anthocyanins and total phenol content between whole fresh 82 fruits, pulps and skins of commercial fig cultivars using mainly spectrophotometric methods. 83 Dueñas et al. 13 showed qualitative and quantitative differences of anthocyanins in pulps and Manuscript 84 skins from Spanish fig cultivars. Oliveira et al.20 found quantitative differences between 85 pulps, skins and leaves of Portuguese fig cultivars, but their study only focused on seven 86 target compounds. 87 Therefore, the obJective of this study was to evaluate the phenolic distribution in Accepted 88 different parts of two Tunisian fig cultivars ‘Temri’ and ‘Soltani’ and give new insights into 89 its contribution to the antioxidant activity using MS-based analysis. To achieve this, dried 90 leaves, whole fruits, skins and pulps were extracted using solid-liquid extraction and analyzed 91 concisely by reversed phase (RP)-ultra-high-performance liquid chromatography (UHPLC) Function 92 coupled to DAD and MS, using a quadrupole-time-of-flight (QTOF) mass analyzer. & 93 Moreover, the total phenol content and the antioxidant activity by means of three in vitro 94 assays were assessed. 95 Food 96 Results and discussion 97 Selection of the extraction procedure 4 Page 5 of 38 Food & Function 98 The first step of the study was to choose an extraction procedure that enabled to 99 recover the maximum amounts of phenolic compounds, but by using the minimum volume of 100 organic solvent and extraction time. In this way, two solid-liquid extraction procedures were 101 tested: a conventional maceration with an ethanolic-aqueous solution (extraction method 1) 102 and an extraction with a methanolic-aqueous solution assisted by an extensive grounding with 103 an Ultraturrax blender and ultrasounds (extraction method 2). In general, our findings showed 104 that the total phenol content (TPC) and antioxidant activity were slightly higher using the 105 extraction method 2, whereas the yield was lower in comparison with method 1 (Fig. 1). 106 Furthermore, the qualitative phenolic profiles using both methods were similar. As an 107 example, Fig. S1 (supplementary information) show the base peak chromatogram (BPC) in Manuscript 108 the negative ionization mode of leaves extracted using the previous methods. These results 109 could be explained by the fact that the solubility of phenolic compounds is quite comparable 110 in both solvents that present similar polarity. 21 Moreover, an exhaustive grounding and a 111 sonication step favored the extraction of phenolic compounds like in previous studies on Accepted 112 different vegetal parts, such as chickpea seeds, lettuce leaves and eggplant fruits, that enable 113 shorting the extraction time.22–24 Interestingly, since ethanol is not as toxic as methanol, the 114 conventional extraction method could be used to prepare bioactive extracts for further in vivo 115 studies, but requiring a higher dosage considering the yield, and the second one is interesting Function 116 for finding key active compounds in a faster and cheaper way.
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