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Single Laboratory Validation of a Quantitative Core Shell-Based LC Single Laboratory Validation of a Quantitative Core Shell-Based LC Separation for the Evaluation of Silymarin Variability and Associated Antioxidant Activity of Pakistani Ecotypes of Milk Thistle (Silybum Marianum L.) Samantha Drouet, Bilal Haider Abbasi, Annie Falguieres, Waqar Ahmad, S. Sumaira, Clothilde Ferroud, Joël Doussot, Jean Vanier, Christophe Hano To cite this version: Samantha Drouet, Bilal Haider Abbasi, Annie Falguieres, Waqar Ahmad, S. Sumaira, et al.. Single Laboratory Validation of a Quantitative Core Shell-Based LC Separation for the Evaluation of Sily- marin Variability and Associated Antioxidant Activity of Pakistani Ecotypes of Milk Thistle (Silybum Marianum L.). Molecules, MDPI, 2018, 23 (4), pp.904. 10.3390/molecules23040904. hal-02538464 HAL Id: hal-02538464 https://hal.archives-ouvertes.fr/hal-02538464 Submitted on 9 Apr 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Distributed under a Creative Commons Attribution| 4.0 International License molecules Article Single Laboratory Validation of a Quantitative Core Shell-Based LC Separation for the Evaluation of Silymarin Variability and Associated Antioxidant Activity of Pakistani Ecotypes of Milk Thistle (Silybum Marianum L.) Samantha Drouet 1,2, Bilal Haider Abbasi 1,2,3 ID , Annie Falguières 4, Waqar Ahmad 3, Sumaira 3, Clothilde Ferroud 4, Joël Doussot 1,2,4, Jean Raymond Vanier 5, Eric Lainé 1,2 and Christophe Hano 1,2,* ID 1 Laboratoire de Biologie des Ligneux et des Grandes Cultures (LBLGC), INRA USC1328, Université d’Orléans, Pôle Universitaire d’Eure et Loir, 21 rue de Loigny la Bataille, 28000 Chartres, France; [email protected] (S.D.); [email protected] (B.H.A.); [email protected] (J.D.); [email protected] (E.L.) 2 Bioactifs et Cosmétiques, GDR 3711 COSMACTIFS, CNRS/Université d'Orléans, 45100 Orléans, France 3 Department of Biotechnology, Quaid-i-Azam University, Islamabad 45320, Pakistan; [email protected] (W.A.); [email protected] (S.K.) 4 Ecole Sciences industrielles et technologiques de l’information (SITI), Département Chimie Alimentation Santé Environnement Risque (CASER), Le CNAM 75141 Paris Cedex 03, France; [email protected] (A.F.); [email protected] (C.F.) 5 Plantes Médicinales et Aromatiques 28, PMA28, 1, place de l’Eglise, 28140 Varize, France; [email protected] * Correspondence: [email protected]; Tel.: +33-237-309-753 Received: 21 February 2018; Accepted: 13 April 2018; Published: 14 April 2018 Abstract: Fruits of Silybum marianum (L.) Gaernt are the main source of taxifolin derived flavonolignans. Together, these molecules constitute a mixture called silymarin with many useful applications for cosmetic and pharmaceutic industries. Here, a validated method for the separation of the silymarin constituents has been developed to ensure precision and accuracy in their quantification. Each compound was separated with a high reproducibility. Precision and repeatability of the quantification method were validated according to the AOAC recommendations. The method was then applied to study the natural variability of wild accessions of S. marianum. Analysis of the variation in the fruits composition of these 12 accessions from Pakistan evidenced a huge natural diversity. Correlation analysis suggested a synergistic action of the different flavonolignans to reach the maximal antioxidant activity, as determined by cupric ion reducing antioxidant capacity (CUPRAC) and ferric reducing antioxidant power (FRAP) assays. Principal component analysis (PCA) separated the 12 accessions into three distinct groups that were differing from their silymarin contents, whereas hierarchical clustering analysis (HCA) evidenced strong variations in their silymarin composition, leading to the identification of new silybin-rich chemotypes. These results proved that the present method allows for an efficient separation and quantification of the main flavonolignans with potent antioxidant activities. Keywords: antioxidant activities; core shell column; ecotypes; LC-MS; Silybum marianum; silymarin Molecules 2018, 23, 904; doi:10.3390/molecules23040904 www.mdpi.com/journal/molecules Molecules 2018, 23, 904 2 of 18 1. Introduction The fruit of milk thistle (Silybum marianum L.) is a rich source of phytochemicals compounds with multiple biological interest. Among them, silymarin is accumulated in the pericarp (the most external part of the fruit) up to 9% (w/w) and it is composed of a mixture of flavonolignans: silybin A, silybin B, silydianin, silychristin, isosilybin A, and isosilybin B, deriving from taxifolin their common flavone precursor (Figure1)[1–7]. Figure 1. Chemical structure of the main six flavonolignans and one flavonoid (*) constituting the Silymarin mixture from Silybum marianum achene extract. Milk thistle has been used as a medicinal plant for centuries as a remedy for various diseases [8,9]. Its extract is used as food supplements based on its traditional use in the European pharmacopoeia as liver detoxifier [10] and as an antidote against Amanita phalloides intoxication [11,12]. Those effects have been related to its well-known hepatoprotective action [2–4,13,14], limiting acute liver injuries thanks to pronounced anti-inflammatory actions and antioxidant activity [15], which is described at both the cellular and molecular levels [16]. Its main constituent Silybin have been largely studied and proposed to display various health promoting effects, such as hypocholesterolaemic action [17] or potential chemopreventive action in human prostate carcinoma [18]. Topical applications of silybin also display a large array of beneficial actions on skin: anti-inflammatory [19], protection against UV-B radiations and sun burns [20–22], antiglycation action [23], and prevention of skin cancers [24]. All of those biological activities evidence the great potential of Silybum marianum extracts for pharmaceutical and cosmeceutical applications. Unfortunately, as reported by Chambers et al. [25], in most of the studies dealing with biological activities of S. marianum extract, their composition is rarely determined. Since silymarin content and composition greatly vary in large amounts depending Molecules 2018, 23, 904 3 of 18 on the extraction procedure, the genetic background, and/or the edaphic parameters, this could result in reproducibility and validity issues [25]. From a chemical point of view, silymarin is composed of different isomers that are difficult to separate. This could explain why, in many cases, publications that are dealing with the elucidation of S. marianum biological activities, silymarin is usually quantified as a whole whereas the relative amounts of the different constituents can vary and are not measured. Among these different constituents, silybins are the major bioactive component of S. marianum extract [6,7], thus reinforcing the need of validated (quantitative) methods for the accurate evaluation of their concentration levels. The understanding of the flavonolignans biosynthesis is currently an important factor to progress in the use of these molecules. Learning more about the natural genetic influencing flavonolignans accumulation is an important step. Native from the Mediterranean area, S. marianum propagates through the world with a vigorous growth in warm and dry regions [2,26]. It was observed to develop locally adapted subpopulations, which are also known as ecotypes, which can differ by their phenotype, growth, tolerance for temperature, light, nutrients, and/or stress [27]. These ecotypes also displayed a wide range of variation in their silymarin content and composition, as described for ecotypes from Egypt, Iran, Poland, Hungary, Bulgaria, Germany, Canada, and New Zealand [25,28–32]. Because of the very rapid propagation of this plant, milk thistle has become a widespread weed, especially in north Pakistan, being widely used by phytomedicine industry [32]. However, variability in silymarin concentration and composition of wild S. marianum accessions from Pakistan have never been studied. Investigating the content of various ecotypes would help to discover the best plants for phytomedicine and cosmetic applications. In this context, optimizing the accurate and quantitative separation protocol for these compounds in a simple way is essential to facilitate their further exploration. For this purpose, we have first developed and validated a quantitative and reproducible LC-based method for the separation of the different flavonolignans from S. marianum fruits using core-shell technology. Subsequently, this method was applied to investigate the natural variability in the silymarin content of wild populations of S. marianum, which are grown in Pakistan in order to enhance our current understanding of the chemical diversity and to estimate associated antioxidant capacities of these compounds. 2. Materials and Methods 2.1. Plant Material The achenes of Silybum marianum of Pakistani purple ecotypes were collected by the Department of Biotechnology from Quaid-i-Azam University and identified
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