Genetic Differentiation in Anthocyanin Content Among Berry Fruits
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Article Genetic Differentiation in Anthocyanin Content among Berry Fruits Alicja Ponder , Ewelina Hallmann * , Martyna Kwolek, Dominika Srednicka-Tober´ and Renata Kazimierczak Department of Functional and Organic Food, Institute of Human Nutrition Sciences, Warsaw University of Life Sciences, Nowoursynowska 159c, 02-776 Warsaw, Poland; [email protected] (A.P.); [email protected] (M.K.); [email protected] (D.S.-T.);´ [email protected] (R.K.) * Correspondence: [email protected]; Tel.: +48-22-59-37-036 Abstract: Anthocyanins are widely distributed secondary metabolites that play an essential role in skin pigmentation of many plant organs and microorganisms. Anthocyanins have been associated with a wide range of biological and pharmacological properties. They are also effective agents in the prevention and treatment of many chronic diseases. Berries are particularly abundant in these compounds; therefore, their dietary intake has health-promoting effects. The aim of this study was to identify and determine the anthocyanin content in selected species and cultivars of berry fruits, such as raspberry, blackberry, red currant, blackcurrant, and highbush blueberry, widely consumed by Europeans. The concentrations of anthocyanins were determined by HPLC, identifying individual compounds: cyanidin-3-O-glucoside, pelargonidin-3-O-glucoside, delphinidin- 3-O-glucoside, delphinidin-3-O-rutinoside, cyanidin-3-O-rutinoside, delphinidin-3-O-galactoside, cyanidin-3-O-galactoside, and malvidin-3-O-galactoside. The experimental data showed that the Citation: Ponder, A.; Hallmann, E.; Kwolek, M.; Srednicka-Tober,´ D.; selected species and cultivars of berry fruits differ significantly in the contents of anthocyanins. Kazimierczak, R. Genetic Among all species tested, blackberry and blackcurrant were characterized significantly by the highest Differentiation in Anthocyanin content of anthocyanins (sum), while the lowest content was found in red currant fruits. Additionally, Content among Berry Fruits. the content of individual anthocyanin compounds in particular species and cultivars was also Curr. Issues Mol. Biol. 2021, 43, 36–51. different. Considering the high content of anthocyanins and their potential positive impact on human https://doi.org/10.3390/ health and protection against disease, berries should be part of healthy nutrition. cimb43010004 Keywords: anthocyanin; bioactive compounds; HPLC method; berry fruits; raspberry; blackberry; Academic Editor: Hany A. El-Shemy red currant; blackcurrant; highbush blueberry Received: 30 March 2021 Accepted: 27 April 2021 Published: 29 April 2021 1. Introduction Publisher’s Note: MDPI stays neutral Anthocyanins are widely distributed secondary metabolites that play an essential role with regard to jurisdictional claims in in skin pigmentation of many plant organs and microorganisms [1]. They are flavonoids published maps and institutional affil- by classification, sharing the same diphenylpropane skeleton (C6C3C6) (Figure1), and are iations. predominantly found in berry fruits [2]. Actually, 25 different anthocyanidins are known, which differ from each other in the presence of hydroxyl (−OH) and methoxy (−OCH3) groups bound at the scaffold core [3]. These compounds have an important function for the quality control of foods that claim to contain specific anthocyanin-enriched fruits. The characteristic anthocyanin pattern is specific for each fruit. Based on this fingerprinting, it Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. is possible to recognize the adulteration and/or sophistication of particular products that This article is an open access article claim to contain a certain fruit. This method allows for the detection of a misidentification distributed under the terms and of the initial plant raw material or adulteration with other plants [3–6]. conditions of the Creative Commons Anthocyanins are water soluble, and their spectral properties are usually responsible Attribution (CC BY) license (https:// for the red, blue, and purple coloring of different plant parts (flowers, fruits, and other creativecommons.org/licenses/by/ plant tissues). This is due to the accumulation of anthocyanins in the flesh and skin of the 4.0/). fruit [7,8]. In the case of fruits like peaches, apricots, plums, and grape berries, anthocyanins Curr. Issues Mol. Biol. 2021, 43, 36–51. https://doi.org/10.3390/cimb43010004 https://www.mdpi.com/journal/cimb Curr. Issues Mol. Biol. 2021, 43 37 accumulate more in the skin than in the flesh [1]. Their specific color depends on the environmental pH and the presence, at the same time, of other compounds from flavone and flavonol groups and metal ions [9]. Depending on the pH value, anthocyanins can exist in many different protonated, deprotonated, hydrated, and isomeric forms. Due to changes in protonation and hydration at acidic pH (pH 1–3), anthocyanins are red; at pH 4–5, they are colorless or yellow; and at pH values between 6 and 7, they became blue-purple [10–12]. The role of anthocyanins in plants is in attracting plant pollinators and increasing stress tolerance. Floral color and scent are the traits that attract pollinators. Anthocyanins provide flowers with radiance and attractiveness, which can act as a beneficial visualization signal to pollinators, increasing the number of pollinator visits and thereby increasing the pollinator foraging efficiency and reproductive success. Additionally, apart from the floral parts, anthocyanins often occur transiently in the root, stem, fruits, and leaf tissues of plants at specific developmental stages in response to unfavorable environmental factors, including Curr. Issues Mol. Biol. 2021, 1, FOR PEER REVIEW 2 UV radiation, cold temperatures, and water stress. They play an important role in the natural protective mechanism of plants [3,13]. FigureFigure 1. Diphenylpropane 1. Diphenylpropane skeleton skeleton (C6 (CC36CC6)3 Cof6 )all of flavonoids. all flavonoids. AnthocyaninsMoreover, fruits, are water especially soluble, berries, and their are spectral particularly properties abundant are usually in different responsible bioactive forcompounds, the red, blue, in and that purple anthocyanins. coloring The of di beneficialfferent plant effects parts of these(flowers, compounds fruits, and for other human planthealth tissues). have This been is known due to fromthe accumulation at least the 16th of anthocyanins century [10]. in There the flesh are a and great skin number of the of fruitstudies [7,8]. devotedIn the case to theof fruits different like biologicalpeaches, apricots, effects exerted plums,by and anthocyanins. grape berries, Anthocyanins anthocya- ninshave accumulate been associated more in with the askin wide than range in the of biological flesh [1]. Their and pharmacological specific color depends properties. on the They environmentalare also effective pH and in the the prevention presence, at and the treatment same time, of manyof other chronic compounds diseases from [11 –flavone14]. They andexhibit flavonol antioxidant groups and activity metal and ions inactivating [9]. Depending properties on the against pH value, free anthocyanins radicals; moreover, can existanthocyanins in many different can provide protonated, anti-inflammatory, deprotonated, antiviral, hydrated, and and anticancer isomeric forms. effects Due [14]. to The anticancer activity of anthocyanins contained in food results from their properties consist- changes in protonation and hydration at acidic pH (pH 1–3), anthocyanins are red; at pH ing of binding of mutagens, inhibiting metabolic activation of pro-mutagens, removing 4–5, they are colorless or yellow; and at pH values between 6 and 7, they became blue- free radicals, inhibiting cancer cell proliferation, intensifying DNA repair processes, and purple [10–12]. The role of anthocyanins in plants is in attracting plant pollinators and inducing apoptosis of cancer cells. They can also influence cell differentiation, exhibit increasing stress tolerance. Floral color and scent are the traits that attract pollinators. An- cytotoxic and cytostatic effects against cancer, and regulate the immune system [14]. thocyanins provide flowers with radiance and attractiveness, which can act as a beneficial Nevertheless, anthocyanins are also used in the development of food colorants and visualization signal to pollinators, increasing the number of pollinator visits and thereby functional ingredients in food. However, the use of anthocyanins as food colorants and increasing the pollinator foraging efficiency and reproductive success. Additionally, apart functional foods ingredients is limited because of the low stability of anthocyanins under from the floral parts, anthocyanins often occur transiently in the root, stem, fruits, and leaf the environmental conditions (heat, oxygen, and light among others) experienced during tissues of plants at specific developmental stages in response to unfavorable environmen- processing and storage [11,15,16]. The anthocyanin content depends on the balance between tal biosynthesisfactors, including and degradation.UV radiation,Genetic, cold temperatures, developmental, and water and stress. environmental They play factors an im- all portantregulate role anthocyanin in the natural metabolism. protective The mechanism genetic differences of plants [3,13]. found in raw materials appear to beMoreover, highly relevant fruits, for especially the anthocyanin berries, contentare part [17icularly]. This abundant