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The Stilbene Profile in Edible Berries

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The Stilbene Profile in Edible Berries Phytochem Rev https://doi.org/10.1007/s11101-018-9580-2 The stilbene profile in edible berries Alfred Błaszczyk . Sylwia Sady . Maria Sielicka Received: 6 November 2017 / Accepted: 7 June 2018 Ó The Author(s) 2018 Abstract Edible berries are becoming increasingly Introduction popular to consume in fresh, dried, frozen or processed forms due to their high content and wide diversity of In recent years, edible berries have attracted much bioactive compounds with considerable health bene- interest due to their high content and wide diversity of fits. Among the wide variety of phytochemicals found bioactive compounds with potential health benefits in berries are stilbenes, which demonstrate a broad (Zhao 2007; Seeram 2012; Jimenez-Garcia et al. 2013; range of biological and pharmacological activities. Nile and Park 2014). Berry fruits are widely consumed Their content depends on many factors, including the in fresh, dried, frozen forms or as processed products, cultivar, ripening stage, climatic conditions, agro- including canned fruits, beverages, jams and yogurts. nomic management, storage conditions and posthar- The most consumed berries are red raspberries (Rubus vest management. However, the application of various idaeus), strawberries (Fragaria x ananassa), black- abiotic and biotic external stimuli could be a strategy berries (Rubus spp.), blueberries (Vaccinium corym- for increasing the production of stilbenes in edible bosum), black currants (Ribes nigrum), red currants berries. To date, several different elicitors, as inducers (Ribes rubrum), chokeberries (Aronia melanocarpa), of plant secondary metabolite stilbenes, have been cranberries (Vaccinium macrocarpon), grapevines applied in different studies. This review focuses on the (Vitis vinifera L. and other Vitis species), bilberries isolation and identification of stilbenes from edible (Vaccinium myrtillus L.), deerberries (Vaccinium berries and presents the influence of different external stamineum L.), cowberries (Vaccinium vitis-idaea stimuli on their profile in grapes. L.), passion fruits (Passiflora edulis) and tomatoes (Lycopersicon esculentum Mill.). Keywords Stilbenes Á Edible berries Á External Among the wide variety of phytochemicals found stimuli in berries are stilbenes. These molecules occur within a limited group of plant families, which have the gene encoding the enzyme stilbene synthase (STS,EC 2.3.1.95). Biosynthesis occurs via the phenylalanine pathway, where phenylalanine ammonia lyase (PAL), cinnamate-4-hydroxylase (C4H), coumaroyl-CoA A. Błaszczyk (&) Á S. Sady Á M. Sielicka ligase (4CL) and STS play a core role in the synthesis. ´ Faculty of Commodity Science, Poznan University of (Fig. 1) A transcriptional factor, Myb14, has been Economics and Business, al. Niepodległos´ci 10, 61-875 Poznan´, Poland found to regulate the expression of STS (Holl et al. e-mail: [email protected] 123 Phytochem Rev Fig. 1 Early stages of stilbene biosynthesis. PAL phenylalanine ammonia lyase, C4H cinnamate-4- hydroxylase, 4CL coumaroyl-CoA ligase, CHS chalcone synthase, STS stilbene synthase 2013). Chalcone isomerase (CHI) is responsible for This review focuses on stilbenes as a specific class the conversion of chalcone to flavanones. On the other of non-flavonoid phenolic compounds present in hand, resveratrol O-methyltransferase (ROMT)is edible berries. The aim of this review is to summarize involved in the methylation of resveratrol. Stilbenes the isolation and identification methods applied for are biosynthesized and accumulate into lipid vesicles stilbenes present in edible berries as well as the in the cytoplasm. Their content can be determined by influence of external stimuli on the quantitative and many factors, including the cultivar, ripening stage, qualitative composition of stilbenes in edible berries. climatic conditions, soil type, agronomic manage- ment, storage conditions and postharvest management (Dixon and Paiva 1995; Castrejon et al. 2008). Due to Molecular structures of stilbenes found in berry the potential health benefits, stilbenes in edible fruits fruits are of high interest. These compounds have demon- strated a wide range of biological and pharmacological The stilbene structure is characterized by two aromatic activities, including anti-tumoural (Bai et al. 2010; rings linked by a double bond, of which the E isomer is Tsai et al. 2017), anti-viral (Nguyen et al. 2011), anti- the most common configuration. They can be found in inflammatory (Zhang et al. 2010), anti-atherogenic berry fruits as monomers, dimers and more complex (Ramprasath and Jones 2010), anti-aging (Kasiotis oligomers (Figs. 2, 3, 4, 5, 6, 7). According to a current et al. 2013) and neuroprotective (Lin and Yao 2006) paper, the most widely found monomeric stilbenes in effects. berry fruits are E-resveratrol (1) and E-piceid (3) 123 Phytochem Rev apoplasm and protection from peroxidative degrada- tion (Morales et al. 1998). The oligomeric stilbenes are formed due to the oxidative coupling of E-resveratrol (1) or other monomeric stilbenes catalysed by perox- idase isoenzymes localized in the vacuole, cell wall and apoplast of grapevine cells (Ros Barcelo et al. 2003). Isolation and identification of stilbenes in edible berries The isolation and identification of stilbenes in edible berry extracts constitutes a complex procedure due to Fig. 2 Molecular structures of E-stilbene monomers isolated from edible berries: 1: E-resveratrol (3,40,5-trihydroxy-E- complex composition of the matrices in which their stilbene), 2: 3,5-O-dimethyl-E-resveratrol (E-pterostilbene), 3: occur, their low concentration and structural com- E-resveratrol-3-O-b-D-glucopyranoside (E-piceid), 4: 3,30,4,5- plexity. Several strategies have been applied for the tetrahydroxy-E-stilbene (E-piceatannol), 5: E-piceatannol-3-O- isolation and identification of stilbenes in edible b-D-glucopyranoside (E-astringin), 6: isorhapontin berries. An overview of the preparation conditions, analytical methods and stilbene concentrations in accordance with the research objectives are presented in Table 1. In general, the extraction techniques applied in stilbene extraction are classified into two categories: conventional and green techniques. The conventional techniques involve soaking in solvent, which relies on the solubility of stilbenes from edible berries in the solvent at room or elevated temperature. These techniques consume a large volume of solvents and are usually time consuming. In contrast, the green extraction technique applies minimal volumes of solvent and requires a shorter time. It has been used as preparation procedure by Ehala et al. (2005)to isolate E-resveratrol from bilberry via microwave- Fig. 3 Molecular structures of Z-stilbene monomers isolated assisted extraction. In conventional extraction tech- from edible berries: 7: Z-resveratrol, 8: Z-resveratrol-3-O-b-D- glucopyranoside (Z-piceid), 9: Z-piceatannol-3-O-b-D-glu- niques of stilbenes from edible berries solid–liquid copyranoside (Z-astringin) extraction of lyophilized, air-dried, frozen or fresh samples with different solvents is applied (see (Fig. 2). Their Z- and E-isomers mainly accumulate in Table 1). Unfortunately, there are no studies in which the berry skin during all stages of development the influence of matrices (lyophilized, air-dried, (Jeandet et al. 1991). E-isomer plant stilbenes may frozen, fresh) on the presence of stilbenes was undergo several types of modifications, such as examined. From a quantitative point of view, the isomerisation, glycosylation, methoxylation, and results obtained by different extraction solvents can- oligomerization (Chong et al. 2009). Due to these not be compared because solvents of different natures modifications, different derivatives of stilbenes are have different extractabilities. Basing on the analysed formed in edible berries from dimers to hexamers works (Table 1), the most often used solvent for the (Figs. 2, 3, 4, 5, 6, 7). In plants, these metabolites extraction process is methanol or the mixtures of generally accumulate in both free and glycosylated methanol with other solvents. In the research con- forms. Glycosylation of stilbenes could be involved in ducted by Sun et al. (2006) and Romero et al. (2001) their storage, transport from the cytoplasm to the the influence of extraction solvents on the amount of 123 Phytochem Rev Fig. 4 Molecular structures of stilbene dimers isolated from 15: pallidol, 16: pallidol-3-O-glucoside, 17: ampelopsin D, 18: edible berries: 10: E- and Z-e-viniferin, 11: E- and Z-d-viniferin, caraphenol B, 19: ampelopsin B 12: E- and Z-x-viniferin, 13: scirpusin B, 14: parthenocissin A, extracted stilbenes was examined. Based on Sun et al. Therefore, the preparation procedure of stilbenes work (Table 1, entry no. 15), methanol acidified with isolation should be carried out in the dark due to the 0.1% HCl was the best solvent to extract specific light sensitivity of double bond in stilbenes. stilbenes from grape skins and seeds. In the research Few studies have dealt with the influence of conducted by Romero et al. (2001) the influence of ultrasound on the resveratrol extraction efficiency temperature and time of extraction on stilbenes from grapes (Burin et al. 2014; Babazadeh et al. 2017). content was examined. The highest extraction of E- The ultrasonication-assisted extraction of resveratrol resveratrol and piceid isomers was observed at 60 °C showed more efficiency than the conventional solvent for 30 min with 80% ethanol. Z-Resveratrol was not extraction with 80% ethanol
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