FRIN-04338; No of Pages 13 Food Research International xxx (2012) xxx–xxx
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Review
Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics Sandra Neli Jimenez-Garcia a, Ramon Gerardo Guevara-Gonzalez a, Rita Miranda-Lopez b, Ana Angelica Feregrino-Perez c, Irineo Torres-Pacheco a, Moises Alejandro Vazquez-Cruz a,⁎ a
Division de Estudios de Posgrado, C.A. Ingenieria de Biosistemas, Facultad de Ingenieria, Universidad Autonoma de Queretaro, C.U. Cerro de las Campanas S/N, Colonia Las Campanas, C.P. 76010, Santiago de Queretaro, Queretaro, Mexico Departamento de Ingeniería Bioquímica, Instituto Tecnológico de Celaya, Av. Tecnológico esq. García Cubas s/n, Celaya, Gto. C.P. 38000, Mexico c Facultad de Medicina, Universidad Autonoma de Queretaro, Clavel #200, Fraccionamiento Prados de la Capilla, C.P. 76176, Santiago de Queretaro, Queretaro, Mexico b
a r t i c l e
i n f o
Article history: Received 29 September 2012 Accepted 6 November 2012 Available online xxxx Keywords: Secondary metabolites Bioactive compounds Sensory profile Human health Quality
a b s t r a c t This review summarizes biological active compounds of berry fruits and their importance in relation to human health. The group of bioactive compounds consists of phenolic compounds, including anthocyanins, phenolic acids, stilbens, tannins, and carotenoids. Berries are important sources of a wide variety of bioactive compounds. Under stress conditions, reactive oxygen species (ROS) and free radicals are produced in an extensive range during metabolism in plants. The insufficiency of antioxidant defense mechanisms in humans is associated to cardiovascular diseases, diabetes, and cancer. The extraction and characterization of bioactive compounds that may help to prevent these disorders and, as a consequence, delay the onset of aging is receiving major attention by researchers along with the generation of a detailed picture of the changing metabolic profiles during berries development. The studies regarding the bioavailability and potential toxicity of bioactive compounds also take part in this review. Finally, we would like to emphasize the importance of associate new plant breeding techniques and genetic studies in berry fruits. The promising research of quality trait loci (QTLs) during the analyses of expression and over-expression of bioactive compounds under controlled conditions in order to obtain value-added fruits for human health is also mentioned. © 2012 Elsevier Ltd. All rights reserved.
Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2. Bioactive compounds in berries . . . . . . . . . . . . . . . . . . . . 3. Factors affecting bioactive compounds content and stability . . . . . . 4. Characterization techniques of bioactive compounds . . . . . . . . . . 5. Sensory analysis of berry compounds . . . . . . . . . . . . . . . . . 6. Health benefits and bioavailability of berry compounds . . . . . . . . 7. Applications of berry bioactive compounds in pharmaceutical industry . . . 8. Effect of processing conditions on bioactive compounds characteristics . . 9. Metabolomic engineering of berry bioactive compounds . . . . . . . . 10. Quality trait locus related to bioactive compounds production in berries . 11. Future challenges . . . . . . . . . . . . . . . . . . . . . . . . . . 12. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
⁎ Corresponding author. Tel.: +52 1 442 1921200x6093. E-mail address:
[email protected] (M.A. Vazquez-Cruz).
The positive relationship between diet and health has increased consumer demand for more information related to healthy diets, including fruits and vegetables, with functional characteristics that
0963-9969/$ – see front matter © 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.foodres.2012.11.004
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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help to delay the aging processes and reduce the risk of various diseases, mainly cardiovascular diseases and cancer, as well as other disorders (Paredes-López, Cervantes-Ceja, Vigna-Pérez, & Hérnandez-Pérez, 2010). The metabolic activity of bioactive compounds is manifested mainly by the scavenging ability of reactive oxygen species (ROS) (Szajdek & Borowska, 2008). Fruits like berries may be an important component of a healthy diet because of their bioactive compounds content. Important berries such as: blackberry (Rubus sp.), bilberry (Vaccinium myrtillus), blackcurrant (Ribes rugrum), blueberry (V. corymbosum), chokeberry (Aronia melanocarpa), cranberry (V. macrocarpon), bayberry (Myrica sp.), raspberry (R. ideaus), black raspberry (R. occidentalis), and strawberry (Fragaria ananassa) are important sources of bioactive compounds usually consumed in fresh and processed products in the human diet (Côté, Caillet, Doyon, Sylvain, & Lacroix, 2010; Garzón, Riedi, & Schwartz, 2009; Ścibisz & Mitek, 2009). Among the chemical compounds found in this type of fruits are the phenolic compounds, being the major group of phytochemicals including flavonoids (anthocyanins, flavonols, flavones, flavanols, flavanones, and isoflavonoids), stilbenes, tannins, and phenolic acids (Tulipani et al., 2008). Diverse studies have shown that biotic and abiotic factors play an important role in the levels of bioactive compounds in berries and their antioxidant activity (Zhang, Seeram, Lee, Feng, & Herber, 2008). The phenolic compounds contribute to protection against degenerative diseases, and their effects on health have been commonly attributed to their antioxidant properties (Seeram, 2008). Improvement in knowledge on their bioavailability is an important step to understand the possible mechanisms of action and their impact on human health (Szajdek & Borowska, 2008). The aim of this review was to provide an overview of the main bioactive compounds in berry fruits and the techniques used for their extraction, purification, characterization and health-promoting properties to emphasize the importance of berry fruits in diet and in the prevention of various diseases. This paper is organized in three main parts: the first briefly presents biochemical composition of berry fruits, in the second part, various biotechnological techniques used for the analysis of berry fruits are described, and finally, the importance of genomics to illustrate how genes (QTLs) affect composition and sensory traits in berry fruits is discussed, remarking their importance in consumption and health promoting effects. 2. Bioactive compounds in berries Berry fruits are characterized by a high content and wide diversity of bioactive compounds such as phenolic compounds, organic acids, tannins, anthocyanins, and flavonoids (Szajdek & Borowska, 2008). The chemical structure of phenolic compounds is characterized by one or more aromatic rings with hydroxyl groups. They are classified by structural characteristics in 5 major groups: phenolic acids, stilbenes, flavonoids (flavonols or catechins, flavonols, flavones, flavonones, isoflavonoids, anthocyanins), tannins and lignans (Han, Shen, & Lou, 2007; Paredes-López et al., 2010). Plants produce an important and diverse assortment of organic compounds, some of them do not appear to be involved in their development. These compounds traditionally referred to as secondary metabolites, often are distributed among limited taxonomic groups within the plant kingdom. Secondary metabolites play an important role in plant adaptation and defense under different stress conditions such as: drought, UV radiation, pathogens and plagues (Dietrich, Rechner, & Patz, 2004; Szajdek & Borowska, 2008). The content of phenolic compounds in berry fruits is determined by many factors, such as the cultivar, agronomic management, climatic factors, ripening stage, harvesting time, storage conditions, and postharvest management (Castrejón, Eichholz, Rohn, Kroh, & Huyskens-Keil, 2008). An example of the aforementioned is the compound called resveratrol, a chemical compound found in the skin of grapes which inhibits the growth of fungi (Han et al., 2007). Researchers have shown that berry fruits
which grow in a cold climate without fertilizers and pesticides are characterized by a higher content of polyphenols than those growing in a milder climate (Szajdek & Borowska, 2008). In addition to protective functions, phenolic compounds, in particular anthocyanins are responsible for the pigmentation of flowers, fruit and leaves (Kähkönen et al., 1999; Szajdek & Borowska, 2008). An excessive content of polyphenols, in particular tannins, may have adverse consequences because it inhibits the bioavailability of iron (House, 1999) and thiamine (Tamir & Alumot, 2006; Veloz-Garcia et al., 2010). The significance of phenolic compounds is recognized as components which may possess many health benefits (Szajdek & Borowska, 2008). Anthocyanins are an important group among polyphenols in berry fruits. A high concentration of anthocyanins is reported in chokeberry, bilberry, honeyberry, blackcurrant, grapes, blackberry, and berrycactus. Anthocyanins in berry fruits comprise a large group of water-soluble pigments. They can be found mainly in the external layer of the pericarp (the skin) (Paredes-López et al., 2010). Anthocyanins comprise aglycones – anthocyanidins and their glycosides – anthocyanins (Viskelis et al., 2009). They form a highly differentiated group of compounds. Anthocyanins differ in the number of hydroxyl groups, the degree of methylation of these groups; the type, number, and place of attachment of sugar molecules, and the type and number of aliphatic or aromatic acids attached to sugars in an anthocyanin molecule (Dugo, Mondello, Errante, Zappia, & Dugo, 2001). In berry fruits, anthocyanins are found in the form of mono-, di- or tri-glycosides, where glycoside residues are usually substituted at C3 or less frequently, at C5 or C7. The most prevalent sugars are glucose, galactose, rhamnose, arabinose, rutinose, sambubiose, and sophorose (Battino et al., 2009; De Ancos, Ibañez, Reglero, & Cano, 2000). Anthocyanin glycoside residues are often acylated by acids: p-coumaric acid, caffeic acid, ferulic acid, and by p-hydroxybenzoic acid, malonic acid or acetic acid (Viskelis et al., 2009). Both the content of anthocyanins and their qualitative composition in berry fruits are determined by the species of the fruits (Table 1). In berries the major phenolic acids are cinnamic and benzoic acid derivatives (Slimestad, Torskangerpoll, Nateland, Johannessen, & Giske, 2005). They occur mainly attached to esters or glycosides. Benzoic acid derivatives such as: p-hydroxybenzoic acid, salicylic acid, gallic acid, and ellagic acid were found in berry fruits (Zadernowski, Naczk, & Nesterowicz, 2005). Chokeberry is a rich source of hydroxycinnamic acid derivatives. They are represented mainly by caffeic acid derivatives, chlorogenic acid and neochlorogenic acid. In chokeberry fruit, the content of those acids reaches 301.85 mg/100 g and 290.81 mg/100 g DW (dry weight), respectively (Lohachoompol, Mulholland, Srzednicki, & Craske, 2008). Ellagic acid is the predominant acid in strawberries where it accounts for 51% of all acids found in this fruit (Aiyer, Srinivasan, & Gupta, 2008). The total content of ellagic acid determined after acid hydrolysis ranged from 25.01 to 56.35 mg/100 g FW (fresh weight) (Gülçin et al., 2011). According to Häkkinen and Törrönen (2000), ellagic acid is also the predominant phenolic acid in raspberries where it accounts for 88% of all phenolic acids. Important quantities of ferulic acid were found in cranberry and blueberry. Also significant amounts of p-coumaric acid and ferulic acid were reported in bilberry, while blackcurrant was characterized by its high content of p-coumaric acid and caffeic acid (Häkkinen & Törrönen, 2000). Tannins are an important group in berries. They comprise both condensed tannins, known as proanthocyanidins, and esters of gallic and ellagic acid — defined as hydrolysable tannins (Bautista-Ortín et al., 2012). Tannins play an essential role in defining the sensory properties of fresh fruit and derived products. They are responsible for the tart taste and changes in the color of fruit and fruit juice. In fruits rich in anthocyanins, tannins stabilize such anthocyanins by binding to them to form copolymers (Hanlin, Hrmova, Harbertson, & Downey, 2010). Hydrolysable tannins are less frequently encountered and have been found in strawberries, raspberries and blackberries (Holt, Francis, Field, Herderich, & Iland, 2008). The largest quantity of condensed tannins with a high degree of polymerization is found in
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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Table 1 Anthocyanin profile in berry fruits (Szajdek & Borowska, 2008). Species
Anthocyanin profile
Dominant anthocyanin
References
Bilberry (Vaccinium myrtillus)
Delphinidin-3-galactoside, delphinidin-3-glucoside, cyanidin-3-galactoside, delphinidin-3-arabinoside, cyanidin-3-glucoside, cyanidin-3-arabinoside, petunidin-3-glucoside, petunidin-3-galactoside, peonidin-3-galactoside, petunidin-3-arabinoside, peonidin-3-glucoside, malvidin-3-galactoside, malvidin-3-glucoside, malvidin-3-arabinoside, delphinidin-3-sambubioside, cyanidin-3-sambubioside Cyanidin-3-glucoside, cyanidin-3-rutinoside, delphinidin-3-glucoside, delphinidin-3-rutinoside, peonidin-3-rutinoside, malvidin-3-rutinoside Cyanidin-3-galactoside, cyanidin-3-glucoside, cyanidin-3-arabinoside, pelargonidin-3-glucoside, cyanidin-3-xyloside, malvidin-3-glucoside Delphinidin-3-galactoside, malvidin-3-galactoside, malvidin-3-glucoside, malvidin-3-arabinoside, delphinidin-3-arabinoside
Malvidin-3-glucoside, cyanidin-3-glucoside, delphinidin-3-galactoside, cyanidin-3-galactoside
Goiffon, Brun, & Bourrier, 1991. Du, Jerz, & Winterhalter, 2004.
Delphinidin-3-rutinoside
Goiffon et al., 1991. Slimestad & Solheim, 2002. Dugo et al., 2001. Goiffon et al., 1991.
Blackcurrant (Ribes nigrum) Blackberry (Rubus fruticosus) Blueberry (Vaccinium corymbosum) Chokeberry (Aronia melanocarpa) Cranberry (Vaccinium axycoccus)
Raspberry (Rubus idaeus) Strawberry (Fragaria x ananassa)
Cyanidin-3-glucoside
Malvidin-3-arabinoside, malvidin-3-glucoside, malvidin-3-galactoside
Cyanidin-3-galactoside, cyanidin-3-glucoside, cyanidin-3-arabinoside, cyanidin-3-xyloside
Cyanidin-3-galactoside
Cyanidin-3-glucoside, cyanidin-3-galactoside, cyanidin-3-arabinoside, peonidin-3-glucoside, peonidin-3-galactoside, peonidin-3-arabinoside, delphinidin-3-glucoside, petunidin-3-glucoside, malvidin-3-glucoside Cyanidin-3-sophoroside, cyanidin-3-glucoside, cyanidin-3-glucorutinoside, cyanidin-3-rutinoside, pelargonidin-3-sophoroside, pelargonidin-3-glucoside Pelargonidin-3-glucoside, cyanidin-3-glucoside, pelargonidin-3-arabinoside, pelargonidin-3-sukcynyloglucoside, cyanidin-3-sukcynyloglucoside
Peonidin-3-glucoside, cyanidin-3-glucoside
chokeberry (Hanlin et al., 2010). Small quantities of tannins were found in honeyberry and blackberry. According to Foo and Porter (1981), blackberry contains only hydrolysable tannins. The stilbene group includes resveratrol which was initially found in grapes. It occurs as free resveratrol and as derivative, i.e. 3-β-monoD-glucoside (Taware, Dhumal, Oulkar, Patil, & Banerjee, 2010). Small quantities of trans-resveratrol were also found in bilberry, cowberry, redcurrant, cranberry, and strawberry. The content of trans-resveratrol in the aforementioned fruits reaches 6.78 μg/g, 30 μg/g, 15.72 μg/g, 19.29 μg/g, and 3.57 μg/g, respectively (Ehala, Vaher, & Kaljurand, 2005). Also berry fruits contain small quantities of carotenoids (Marinova & Ribarova, 2007). Chokeberry is one of the richest sources of carotenoids which content reaches an average of 48.6 mg/kg FW. Chokeberry fruits contain lycopene, β-carotene, ζ-carotene, β-cryptoxanthin, lutein, 5,6-epoxylutein, trans-violaxanthin, cis-violaxanthin, and neoxanthin (Lashbrooke, Young, Strever, Stander, & Vivier, 2010). 3. Factors affecting bioactive compounds content and stability Water deficit exerts significant effects on berry composition promoting an improvement of quality traits such as color, flavor, and aroma. Some pathways and enzymes affected by water deficit have been identified, little is known about the global effects of water deficit on grape berry metabolism (Deluc et al., 2009). Vitis vinifera L. has relatively high drought tolerance (Grimplet, Deluc, Cramer, & Cushman, 2007). Grape sensitivity to water deficit depends on the timing application being particularly more sensitive during anthesis and just after anthesis (Matthews, 1989). Regulated-deficit irrigation has been used to improve berry and wine quality (Chapman, Roby, Ebeler, Guinard, & Matthews, 2005). For instance, application of water deficit early in the season before veraison, which is the change of color of the grape berries, resulted in higher concentrations of anthocyanins and phenolics
Kader, Rovel, Girardin, & Metche, 1996. Lohachoompol et al., 2008. Oszmiański & Sapis, 1988. Slimestad et al., 2005. Andersen, 1989.
Cyanidin-3-sophoroside
Proteggente et al., 2002 De Ancos et al., 2000.
Pelargonidin-3-glucoside
Skupień & Oszmiański, 2004. Proteggente et al., 2002. Gil et al., 1997.
(Matthews, Ishii, Anderson, & O'Mahony, 1990). Color differences were the result of increased anthocyanin synthesis promoted by water deficit applied either early or late in the season (Castellarin, Matthews, Di Gaspero, & Gambetta, 2007). Application of water deficit after veraison decreases berry weight to a lesser extent, while still increasing substantially phenolic compounds such as anthocyanins (Deluc et al., 2009; Matthews et al., 1990). In addition, the rates of accumulation of flavonoids as well as the degree of tannin polymerization may be increased (Grimplet et al., 2007). Matthews (1989) and Matthews et al. (1990) showed that the growth of berries and the concentration of flavonoids in fruit were inhibited when water deficits were imposed before veraison. Based on the observation of similar flavonoid content among berries between different treatments, Kennedy, Matthews, and Waterhouse (2002) concluded that post-veraison water deficits only inhibited fruit growth. Roby, Harbetson, Adams, and Matthews (2004) analyzed the effects of berry size and of low vine water status on flavonoid concentration to show that there are effects of vine water status on fruit composition that are independent of the inhibition of berry growth (Castellarin et al., 2007). The metabolism of monoterpenes in grapevine is not well understood yet. Biosynthesis of monoterpenes is likely to take place in the berry itself, without the need for translocation from other parts of the plant (Gholimi et al., 1995). The evolution of monoterpene contents during grape maturation seems to be largely variety-dependent (Park and Noble 1993), with some compounds already present before veraison, some starting to accumulate from veraison like linalool (Ebang-Oke, de Billerbeck, & Ambid, 2003), and some keeping accumulating even after sugar/acid maturity while others decrease. QTL detection, simple and composite interval mapping were performed, as well as non-parametric Kruskal–Wallis tests (Fournier-Level et al., 2009). QTLs for muscat score were found on linkage groups (LGs) 1, 5 and 7. For the three ln-transformed monoterpene contents, QTLs with major effects (explaining 17–55% of total
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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phenotypic variance) were found to be colocated on LG 5, on the male and consensus maps. One additional QTL was found for linalool on LG 2, on female and consensus maps, as well as other found for nerol and geraniol on LG 13, on male and consensus maps. These additional QTLs had lower effects (9–25%). The contribution of these results to the knowledge of muscat aroma genetic determinism is discussed, as well as their potential usefulness for marker assisted breeding of new aromatic grape varieties (Doligez, Audiot, Baumes, & This, 2006). 4. Characterization techniques of bioactive compounds The choice of isolation and analytical techniques used for the characterization and/or quantification of bioactive compounds from berries is drive by the chemical structure, the sample particle size, and the presence of interfering substances (Vazquez-Cruz et al., 2012). The chemical nature of berry bioactive compounds ranges from simple to highly polymerized substances which include different proportions of phenolic acids, anthocyanins, and tannins among others. They may also exist in a complex state with carbohydrates, proteins, organic acids, and other plant components forming high-molecular weight phenolics (tannins) and their complexes that are generally insoluble (Côté et al., 2010). Therefore, phenolic extracts obtained from the fruit matrix and plant raw materials are always a mixture of different classes of phenolic compounds which will depend on the solvent system used for the extraction (Lashbrooke et al., 2010). Different techniques can be used to characterize and quantify bioactive compounds in berries, although by far the most widely employed technique has been high-performance liquid chromatography (HPLC) coupled with ultraviolet visible (UV/Vis) and mass spectrometric (MS) detection instruments (Escarpa & Gonzalez, 2000; Merken & Beecher, 2000; Rodriguez-Delgado, Perez, Sanchez, & Montelongo, 2000; Vazquez-Cruz et al., 2012). The recorded phenolic compound content of a sample can be greatly influenced by the method used for analysis. Lee, Rennaker, and Worlstad (2008) have demonstrated the importance of reporting the standard compound used to express the relative concentration values. Several studies employ different methods of extraction, purification, and characterization of the phenolic compounds in berries. Isolation of bioactive compounds from a sample matrix is generally a prerequisite to any comprehensive analytical scheme. Solid phase extraction (SPE) techniques and fractionation based on acidity are commonly used to remove undesirable phenolic and non-phenolic substances or volatile organic compounds (VOC's) (Naczk & Shahidi, 2004; Robbins, 2003; Vazquez-Cruz et al., 2012). The procedure must allow quantitative recovery of the compounds of interest while avoiding any chemical modifications in the analytes which result in artifacts and complicated subsequent steps (Robards & Antolovich, 1997; VazquezCruz et al., 2012). The chemical profile of phenolic compounds from strawberries has been studied using liquid chromatography electrospray ionization mass spectrometry (LC-ESI–MS) methods (Côté et al., 2010). Strawberries were found to contain a wide variety of phenolics such as ellagic acid, ellagic acid glycosides, ellagitannins, gallotannins, flavonols (quercetin and kaempferol glucuronides, and glycosides), anthocyanins (pelargonidin and cyanidin glycosides), flavonols and coumaroyl glycosides (Zhang et al., 2008). Normal-phase chromatography has been used for the separation of flavonoids in food, but with this system it is probably that highly polar materials may be irreversibly retained on the column, resulting in a gradual alteration of the separation characteristics. Thus, reversedphase chromatography (RP-C) has been the method of choice for the separation of the phenolic compounds and flavonoids in berries (Escarpa & Gonzales, 2001; Lee, 2000; Merken & Beecher, 2000; Robards & Antolovich, 1997). Since all phenolics contain at least one aromatic ring, they can consequently absorb UV light effectively and each class of phenolics has a distinctive UV or UV–vis spectra (Côté et al., 2010). The
diode-array detection, DAD, set at a specific wavelength for scanning on an entire spectrum (190 to 600 nm), allows the collection of data which provide the unique scan for specific compounds and their maximum wavelength (Lashbrooke et al., 2010). Combined with chromatographic retention properties, these spectral techniques enable compound characterization and rapid diagnosis of certain structural features of each eluted compound (Escarpa & Gonzales, 2001; Escarpa & Gonzalez, 2000; Robards & Antolovich, 1997). The typical UV/Vis absorption spectra of hidroxycinnamic acid (HCA) derivatives have peaks between 305 and 330 nm (band I) and shoulders between 290 and 300 nm (band II). Commonly occurring HCA derivatives – ferulic, sinapic, caffeic, and p-coumaric acids – have absorbance maxima at 300 nm (Ibrahim & Barron, 1989; Lee, 2000; Van Sumere, 1989). Most hydroxybenzoic acid (HBA) derivatives display their maximum at 246–262 nm, with a shoulder at 290–315 nm, except for gallic and syringic acids, which have absorbance maxima at 271 and 275 nm, respectively (Côté et al., 2010; Escarpa & Gonzales, 2001). Mass spectrometry detection, MSD, is generally used to determine molecular masses and to establish the distribution of substituents on the phenolic rings (Harnly et al., 2006). Nowadays, MSD consists of different parts such as: an injection port that can accomplish nebulization and vaporization of the liquid sample, an ion source that ionizes the sample, a capillary column for ion transport and fragmentation, a quadrupole which separates the ions according to their mass-to-charge ratio, m/z, and an electron multiplier for ion detection (Lashbrooke et al., 2010). With the development of atmospheric pressure ionization, API, the HPLC–MS coupling has become more efficient and easy to use for the analysis of polyphenolic and phenolic compounds found in berries and other fruits (Cuyckens & Claeys, 2004). 5. Sensory analysis of berry compounds Flavor is given by perception of both taste and odor, which are also modulated by temperature and other sensory inputs. Most flavor compounds interact with odor receptors in the nose, but some of them have also an impact on taste. Many natural aroma compounds have chiral centers and can exist as enantiomeric forms: different enantiomer could have quite different sensory thresholds, or even have different aroma characteristics (Malowicki, Martin, & Qian, 2008). The study of flavor from an analytical and scientific point of view has been achieved by the development and application of modern analytical techniques such as olfactometry (Vazquez-Cruz et al., 2012). Therefore, correlation of qualitative and quantitative compositions of some berry fruits has been well characterized and included among the different traits which describe the fruit quality (Zebatakis & Holden, 1997). Consumer perception of quality is based on sensory attributes. The different amounts of sugars and organic acids largely contribute to taste perception. Berry fruits mainly accumulate hexose sugars (glucose and fructose). These sugar levels depend on maturity stage, genetic, and environmental factors (Viljakainen, Visti, & Laakso, 2002). Analyzing the relationship of sugar and acid levels of berries with consumer expectations would help in developing optimum quality standards for harvesting dates (Jayasena & Cameron, 2008). The aroma of berries is another of the key properties determining their quality. It depends on several factors like climate and soil properties, growing practices, maturity stage and variety (Prosen, Janes, Strlic, Rusjan, & Kocar, 2007; Vazquez-Cruz et al., 2012). Berry fruits produced hundreds of volatile compounds contributing to the overall flavor, concentration and composition of these volatiles which are affected by fruit maturity stage, growing management, and storage conditions (Vazquez-Cruz et al., 2012). The study of biosynthetic pathways of volatile organic compounds (VOCs) is a rewarding field of investigation. VOCs are produced by all plants and fruits (Arroyo, Moreno, Daza, Boianova, & Romero, 2007; Vazquez-Cruz et al., 2012). VOCs are responsible for the aroma of berries in a genus- and species-specific way, e.g.: octoploid strawberry
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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(F. x ananassa) aroma is predominated by esters with alcohols, aldehydes, and ketones present in smaller quantities; ketones and terpenes prevail in the headspace of raspberries (Rubus); as well as for blueberries, V. corymbosum aroma is dominated by aromatic hydrocarbons, esters, terpenes and long chain alcohols, while that of V. angustifolium is mainly composed of esters and alcohols (Aharoni et al., 2004; Jetti, Yang, Kurnianta, Finn, & Qian, 2007). Polyphenols are considered to be the most important compounds affecting flavor in fruits. Polyphenolic compounds play an important role in overall organoleptic properties of fruits. These compounds contribute to the bitterness and astringency of berries and berry juices due to the interaction between procyanidins and the glycoproteins in saliva (Rider, Ikegami, & Jobe, 1992). Sensory evaluation studies showed that tetrameric procyanidins are bitterer, whereas the other high polymeric components are more astringent on an equivalent weight basis (Shi et al., 2005). Grapes contain carotenoids (mainly lutein and β-carotene) which are important aroma precursors. After veraison, grape carotenoids are converted into norisoprenoid compounds, which have been identified as the responsible for typical aroma characteristics (Giovanelli & Brenna, 2007). The most commonly consumed berries are strawberries (Fragaria x ananassa), raspberries (Rubus idaeus), blackberries (Rubus spp.), blueberries (Vaccinum corymbosum), black currants (Ribes nigrum) and red currants (Ribes rubrum). Edible berries have been part of human diet for centuries (Saltmarch, Crozier, & Ratcliffe, 2003). Despite the historical longevity, most types of berries have never been developed beyond local markets, reflecting in part their susceptibility to post-harvest decay (Beattie, Crozier, & Duthie, 2005). Little is known about the genetic determinism of muscat flavor in grape, it has been performed a search for QTLs of both muscat score and berry content in the three main free monoterpene alcohols potentially involved which are linalool, nerol and geraniol, based on two-year-study (Klee, 2010). Parental and consensus framework genetic maps of the cross MTP2687-85 (OlivetteRibol) Muscat of Hamburg were built after genotyping the 174 offspring for 139 wells cattered SSR markers. QTLs for muscat score were found on linkage groups (LGs) 1, 5 and 7. The contribution of these results to the knowledge of muscat aroma genetic determinism is discussed, as well as their potential usefulness for marker assisted breeding of new aromatic grape varieties. In strawberry, no mapping of volatile loci has been published. Strawberry is significantly hindered by the genetics of the octoploid commercial cultivars as well as inbreeding depression. Some volatile related with QTLs have been identified in other fruit crops, including apple (Dunemann, Ulrich, Boudichevskaia, Grafe, & Weber, 2009) and grape (Doligez et al., 2006; Duchene et al., 2009). Other studies have investigated the genetic basis of aroma compounds by a QTL-based approach in grape (Vitis vinifera) (Battilana et al., 2009; Doligez et al., 2006). As a proof of concept show that one homoeolog of the O-methyltransferase gene (FaOMT) is the locus responsible for the natural variation of mesifurane content. Sequence analysis identified 30 bp in the promoter of this FaOMT homologous containing putative binding sites for basic/helix–loop–helix, MYB, and BZIP transcription factors. This polymorphism fully co-segregates with both the presence of mesifurane and the high expression of FaOMT during ripening. Mapping of QTLs controlling fruit aroma and volatile levels and subsequent identification of linked molecular markers is an important goal for future marker-assisted selection (MAS) in strawberry (Constantini, Battilana, Lamaj, Fanizza, & Grando, 2008). Strawberries emit VOCs, of which only a few are the major ones contributing to the characteristic strawberry aroma. The different proportions of the volatile components often determine aroma properties. Strawberry aroma is mainly influenced by a mixture of up to 360 individual esters, aldehydes, ketones, alcohols, terpenes, furanones and sulfur compounds (Kafkas et al., 2005). Studies conducted on different accessions identified both genotype-specific and generally-important VOCs. Because of its high odor activity values, furaneol (4-hydroxy-
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2,5-dimethyl-3(2H)-furanone, HDMF) is the key flavor VOC in strawberry fruits, and its levels strongly increase during fruit ripening (Raab et al., 2006). Methyl anthranilate (MA) is the main volatile compound in several wild strawberries like Fragaria vesca with the dominating odor impact which generates a pleasantly “wood strawberry”-like aroma which is preferred by consumers. Esters are known as important key compounds of strawberry aroma which are responsible for the fruity impressions (Ulrich, Komes, Olbricht, & Hoberg, 2007). Terpenes represent the characteristic compounds of several leaves, fruits, vegetables and essential oils. Very recently Aharoni et al. (2004) reported about lower terpene contents in strawberries. The odor of terpenes ranges from unpleasant impressions like turpentine and resinous to pleasant citrus and flowery notes (Ulrich, Hoberg, Rapp, & Kecke, 1997). The most aromatic strawberry varieties tend to accumulate relatively high levels of esters and furanones during fruit maturation (Kafkas et al., 2005). Another well characterized berry is the blackberry, an aggregate fruit composed of many smaller fruits called drups. The aroma in blackberry is one of the major traits affecting its quality in either fresh fruits or processed products. Furans have been found to be the most abundant aromatic compounds such as 5-hydroxymethylfurfural which has been the major component representing 79.7%–96.1% of the total aroma profile depending on blackberry variety. These data suggested that 5-hydroxymethylfurfural is the most important compound contributing to the characteristic flavor of blackberries (Wang, Bowman, & Ding, 2008; Zadernowski et al., 2005). Also, blackberry fruits are an excellent source of natural antioxidants. Several authors have studied anthocyanin and phenolics content as well as antioxidant capacity in blackberries, and have confirmed that they are a good source of dietary phytochemicals (Moyer, Hummer, Finn, Fret, & Wrolstad, 2002). Wang, Cao, and Prior (1996) reported that blackberry extracts show a high activity against superoxide radicals, and they are used as an auxiliary treatment of some diseases like cancer and leukemia, especially those obtained from thornless variety (Wang et al., 2008). There are several Vaccinum species, which have the common name of cranberry. American cranberry (V. macrocarpon Ait) is the only cranberry having a substantial economical value (Huopalahti, Järvenpää, & Katina, 2000). Cranberries are distinguished by a wide spectrum of bioactive substances. American cranberries contain ascorbic acid (13.7 to 28.5 mg/100 g), phenolics compounds (192.3 to 676.4 mg/100 g), titratable acids (2.2 to 2.3%) and sugars (3.66 to 4.9%) (Uwieczkowska, Kawecki, & Stanys, 2004). Cranberry juice is the main product for the consumption, and has become a popular drink due to its sourness and fresh taste and healthy components. Cranberries and cranberry products are popular because of their attractive red color and mildly astringent flavor which is mainly derived from high concentrations of volatile organic acids (Huopalahti et al., 2000). Cranberry fruit is a rich source of various classes of bioactive phenolic compounds, especially flavonoids (Cunningham et al., 2004). Four phenolic classes identified in cranberries include phenolic acids, anthocyanins, flavonols, and flavan-3-ols, which consist of monomers and polymer classes of proanthocyanidins (Cunningham et al., 2004). Berrycactus is an endemic cactaceae grown in wild areas of Central Mexico that are not usually considered suitable for agricultural activities (Céspedes et al., 2005). Recent research about physicochemical properties of berrycactus focuses on betalains. It has been demonstrated that betalains have important antioxidant properties (Hernandez-Lopez, Vaillant, Reynoso-Camacho, & Guzman-Maldonado, 2008). Concentration and aroma descriptors of chemical compounds are used for determining sensory and chemical composition quality. Major compounds tentatively responsible for berrycactus aroma are furanones: furfural, 5-methyl-2-furancarboxaldehyde, 5-methyl-2(5H)-furanone, and 2(5H)-furanone; furfural is the most abundant and its aroma is describes as caramelized/sweet. Regarding aroma quality, the most pleasant aroma is produced by fresh berrycactus, the compound 2,3-dihydro-3,5-dihydroxy-6-methyl- 4H-pyran-4-one has been
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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reported as an abundant compound of berrycactus. More research is needed in order to establish if this compound could be used as a varietal marker of berries, and if its presence is useful to monitoring the ripening process of berrycactus; both furanones and esters contribute to the aroma of berrycactus (Vazquez-Cruz et al., 2012). 6. Health benefits and bioavailability of berry compounds During the last years various studies have targeted the characterization and utilization of bioactive compounds in, in functional foods, like berries, and their benefic properties for human health based on clinical research (Fig. 1), The World Health Organization (WHO) emphasizes the importance the bioactive compounds, especially from small colorful fruits for prevention of the most important health problems namely cardiovascular diseases, diabetes, cancer, and obesity (Stapleton, James, Goodwill, & Frisbee, 2008). Many phenolic compounds of berries are responsible for the color (i.e. anthocyanins) and flavor (i.e. tannins) of fruits. Some factors such as species, variety, geographic region, storage conditions, ripening stage, climate factors and others may affect the concentration of phenolic compounds in berries (Kellogg et al., 2010). The phenolic compounds protect plants against adverse factors such as pathogens, physical damage, UV radiation, and other factors (Dietrich et al., 2004). For example, the skin of grape contains resveratrol; this stilbene serves as phytoalexin. The major function of resveratrol is to protect plants against fungal infections, especially against infection with Botrytis cinerea (Lee, Zhang, & Sanderson, 2008). On the other hand, the major contribution to the antioxidant capacity of berries of the genus Rubus and Fragaria are the ellagitannins, which represent between 51% and 88% of all phenolic compounds depending on the maturity stage, in fully ripe red fruit concentration of this compounds can be 50% lower (Table 2) (Castrejón et al., 2008). These differences are very important for determining the best harvesting date (Lafay & Gil-Izquierdo, 2008). The later indicates that growth conditions, including stress, may affect the antioxidants levels and should be used to assess antioxidant activity at the harvest time (Brownmiller, Howard, & Prior, 2008). Another important group is the stilbenes, small naturally occurring phenolic compounds found in a wide range of plants; berries are an important source of them. Resveratrol, pterostilbene, and piceatannol are stilbenes found in deerberry, cowberry, blueberry, and lingonberry (Ścibisz & Mitek, 2009). An analogue of resveratrol, pterostilbene, is a more effective antioxidant and hemopreventive agent than resveratrol (Wang et al., 2008). Resveratrol and analogues present important biological properties including anti-inflammatory, antiallergenic, antiaging, algicidal, antimutagenic, anticancerigen, and other activities (Shakibaei, Harikumar, & Aggarwal, 2009). Nowadays, consumers are interested in their personal health along with the sensory attractive characteristics of food. During the last years, in vitro and clinical studies have focused on certain microbial effects in cranberry phenolic compounds (Bodet et al., 2008). Condensed tannins of cranberry can inhibit the adhesion of uropathogenic fimbriated
Fig. 1. Properties supporting the health benefits of berries (Stapleton et al., 2008).
Table 2 Bioactive compounds in berries (Castrejón et al., 2008). Berries
Bioactive compounds
mg/g fresh weight
Bilberry
Phenolic compounds Flavonoids Anthocyanins Phenolic compounds Flavonoids Anthocyanins Phenolic compounds Flavonoids Anthocyanins Phenolic compounds Flavonoids Anthocyanins Phenolic compounds Flavonoids Anthocyanins Phenolic compounds Flavonoids Anthocyanins Phenolic compounds Flavonoids Anthocyanins Phenolic compounds Flavonoids Anthocyanins
525 44 300 486 276 326 585 50 495 315 157 140 652 74 77 121 6 99 1400 9 22 313 – 54
Blackberry
Blueberry
Cramberry
Lingonberry
Raspberry
Redcarrant
Strawberry
Escherichia coli to uroepithelial cells in the urinary tract (Paredes-López et al., 2010). Some extracts of cranberry have been also reported to inhibit the adherence of uropathogenic E. coli as well as the inhibition of the sialic-acid-specific adhesin of Helicobacter pylori to human gastric mucosa, a critical step in gastric ulcer development (Ayala-Zavala, Wang, Wang, & González-Aguilar, 2007). Extracts of cranberry contain high molecular weight compounds that inhibit viral adhesion and infectivity of the A and B influenza viruses (Cunningham et al., 2004). These studies have been supported by clinical experimentation showing that regular consumption of cranberry and its derived products can suppress urinary infections, H. pylori infections in epidemically affected populations, and influenza virus infections, and may have a therapeutic potential (Bodet et al., 2008). Some studies indicate the biophenolic compounds (flavonoid and tannins) may act as a new type of antimicrobials which may control the pathogens and may help to overcome the problems with antibiotic resistance (Szajdek & Borowska, 2008). Another potential use of bioactive compounds is the damage prevention by ROS and free radicals which are produced in an extensive range during metabolic processes. In order to reduce oxidative stress, the human body has developed mechanisms for maintaining redox homeostasis. These mechanisms include the non-enzymatic and enzymatic antioxidant defenses produced in the body (endogenous) and others supplied by the diet (exogenous). The exogenous antioxidants include phenolic acids, flavonoids, stilbens, and tannins (Han et al., 2007). Phenolic compounds exhibit many biologically significant mechanisms of action, such as scavenging or detoxification of ROS, blocking ROS production, impacting cell cycle, suppression of tumors, modulation of signal transduction, apoptosis, detoxifying enzymes and metabolism (Ogawa et al., 2008). Secondary metabolism indicates the beginning of specific stages of development, e.g. anthocyanin accumulation during fruit ripening. bZIP transcription factors like FruitE4 on LG 4 are expressed constitutively or tissue specifically and regulate diverse processes such as photomorphogenesis and light signaling (McCallum et al., 2010) and stress and hormone signaling (Fouenier-Level, Hugueney, Verriès, This, & Ageorges, 2011). Precise roles of transcription factors underlying antioxidant QTL are not clear yet. Data presented have located important QTLs for the major anthocyanins in the Rubus genetic linkage map along with several candidate genes and markers associated with these QTLs. Recent work in Rosaceae species (Zorrilla-Fontanesi et al., 2012) pointed out that transcription factors underlie such QTLs. As berry fruits breeding programs move
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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towards using genetic markers assisted strategies, genes and markers identified here will serve as tools to begin identifying closer associations between genotypes and antioxidants contents with the objective of increasing nutritional value of these berry fruits (Causse, Saliba-Colombani, Lesschaeve, & Buter, 2001; Fouenier-Level et al., 2011). One of the aims of aging research is the isolation and characterization of compounds that delay the onset of aging and thus may prolong lifespan. Among the life-prolonging benefits of resveratrol demonstrated in the study made by Barger et al. (2008) were the increased insulin sensitivity, lower blood glucose levels, enhanced mitochondrial energy production, and improved motor function (Barger et al., 2008). The expression of sirtuin genes is associated with aging and longevity. Resveratrol may affect the activation of sirtuin genes; for this reason, it may be an excellent candidate to be considered as an antiaging compound, however, clinical research is necessary to elucidate the potential of this compound for such function (Lee, Zhang, & Sanderson, 2008). There is an increasing interest for innovative anticancer therapies. Ongoing efforts are searching for novel and effective chemopreventive and chemotherapeutic drugs. Resveratrol has shown in vitro as well as in vivo chemopreventive and chemotherapeutic activities. Many of the signaling pathways involving resveratrol have been evaluated and many of its targets and mechanisms of action have been identified. Indeed, resveratrol has shown chemopreventive and chemotherapeutic activities in all three stages of carcinogenesis (initiation, promotion, and progression) (Barger et al., 2008; Taware et al., 2010). Bioactivity depends on the concentration of a specific component at a physiologically significant level at the target site. The absorption determines the compound bioavailability which is also influenced by the extent at which the compound reaches the circulatory system and is available at the site of action, as well as the distribution of the compound into tissues and organs following absorption. The absorption of phenolic compounds, such as flavonoids from plant foods, is minimal due to majority of flavonoids occurring in a glycosidic form (Lafay & Gil-Izquierdo, 2008). Research on animal has been frequently used to investigate the bioavailability of phenolic compounds. Aiyer et al. (2008) found that 0.7 μM/L of ellagic acid was absorbed in 0.5 h, but 113.4 μM of chlorogenic acid was absorbed in 12 h in rats; this behavior may be due to absorption of ellagic acid in the upper part of the gut, in the stomach and small intestine. Chlorogenic acid is a caffeic acid ester linked to quinic acid, and there are no esterases in human tissues able to hydrolyze chlorogenic acid. Gallic acid is absorbed in the rat stomach in the free form. Generally, absorption and bioavailability are affected by the structure of phenolic compounds (glycosylation, molecular weight and esterification) (Gülçin et al., 2011; Han et al., 2007). McGhie and Walton (2007) applied a dose of 74 mg of the anthocyanin cyanidin-3-glucoside/kg of Marion berry to pigs, and reported maximum concentrations in plasma for the original compound (0.103 μM/L; T max: 60 min), for methylated metabolites (b0.021 μM/L; T max: 15–120 min), and for glucuronidated compounds (b0.07 μM/L; T max: 15–60 min). The glucuronide and methylated conjugates of anthocyanins have been found to be the two major types of metabolites that appear in urine of pigs. The urinary recovery of the original anthocyanins and their related metabolites was 0.088%. The aglycone and the sugar moieties interfered the absorption and metabolism of anthocyanins administered to pigs in this research (Kopjar, Tiban, Pilizota, & Babic, 2009; McGhie & Walton, 2007). These data indicate that anthocyanins may be absorbed in the original or in some modified forms, which are generated by enzymatic transformation after their ingestion (Gil, Holcroft, & Kader, 1997; Paredes-López et al., 2010). The number of studies about the bioavailability of anthocyanins in humans has increased over the last years (Zhao & Moghadasian, 2008). In a study involving healthy humans, when gallic acid was absorbed, regardless the form in which it was consumed (purified form, wine or tea), it was present in methylated and glucuronidated forms (Aiyer et al., 2008). When volunteers consumed 200 ml of
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black tea, gallic acid was rapidly detected in plasma at 1.4–1.5 h and its concentration (aglycone and derivatives) was 4.7 μM. Cartron et al. (2003) showed that gallic acid was found without any structure modification in human plasma at a maximum concentration reached 1.5 h after red wine consumption; perhaps, the food matrix may have not influenced the bioavailability of gallic acid, however, more specific studies are needed to reflect the real situation at the cellular level of the phenolic compounds in plant-supported nutrition. Several reports (Barger et al., 2008; Joseph, Fisher, Cheng, Rimando, & Hale, 2008; Lee, Zhang, & Sanderson, 2008; Shakibaei et al., 2009; Shankar, Singh, & Srivastava, 2007) suggest that the effects of resveratrol are tissue specific. Dai et al. (2007) showed that the stimulatory effect of resveratrol on proliferation of human mesenchymal cells is dose dependent. The concentration of resveratrol at 10.5 M was stimulant, whereas a resveratrol concentration of 10.4 M turned out to have an inhibitory effect on proliferation; this situation shows that clinical studies are needed to indicate the specific dosage for each therapeutic activity. In the short-term kinetics study, quercetin was clearly bioavailable from black currant juice. The quercetin found in plasma is commonly originated from the quercetin-3-glucoside present in black currant juice. On the other hand, quercetin from quercetin-3-rutinoside appears in plasma several hours after ingestion (peak plasma values are achieved between 5 and 10 h) (Shakibaei et al., 2009; Shankar et al., 2007). This demonstrates that quercetin is bioavailable from berries when they are consumed as part of a balanced diet (Nurmi et al., 2009). Several short-term studies have previously shown that quercetin is bioavailable from its main dietary sources like onions (Maiani et al., 2009), tea (Šavikin et al., 2009), and red wine (Cartron et al., 2003; Hanlin et al., 2010). The bioavailability of quercetin during long-term consumption diets resembling those of the general population, with or without berries. The most commonly consumed berries in Finland are lingonberries (Vaccinium vitis idaea), which are like small cranberries, and bilberries (V. myrtillus), closely related to blueberries, are sold frozen in supermarkets all year and are picked by people residing in rural areas (Holt et al., 2008). Black currants, strawberries, and raspberries, which are widely consumed, are cultivated but are also grown by many people in their own gardens. Quercetin is mainly present in plants as glycosides, for example the black currants contain about half and half of quercetin-3glucoside and quercetin-3-rutinoside and small amounts quercetin hexoside-malonate (Lafay & Gil-Izquierdo, 2008). The total quercetin amount, expressed as milligrams aglycone per kilogram of fresh weight of berry, was 47 for black currant. The total quercetin content in lingonberries and bilberries was reported to be 131 and 81 mg/kg, respectively (Paredes-López et al., 2010). The quercetin content of strawberries and raspberries was much lower (Beattie et al., 2005; Bodet et al., 2008). 7. Applications of berry bioactive compounds in pharmaceutical industry Bioactivity depends in the concentration of a given specific component at a physiologically significant level at the target site. The preventive or therapeutic action is affected by its pharmacokinetic properties (absorption, distribution, metabolism, and excretion). The pharmacokinetics of several phenolic compounds has been well documented (Stapleton et al., 2008). The chemical structure of phenolic compounds determines their rate and level of absorption and the nature of the derivatives circulating in the plasma. The absorption determines the compound bioavailability, which is also influenced by the extent to which the compound reaches the circulatory system and is available at the site of action, as well as distribution of the compound into tissues and organs following absorption. Metabolism of bioactive compounds begins as soon as the compounds enter the body, but the majority of them are metabolized in the liver by cytochrome P450 enzymes. The absorption of phenolic compounds, such as flavonoids, from plant foods is minimum given the
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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fact that the majority of flavonoids occur in a glycosidic form (Carbone, Mourgues, Perrotta, & Rosati, 2008; Viskelis et al., 2009). Animal studies have been frequently used to investigate the bioavailability of phenolic compounds. Phenolic compounds in animals are rapidly absorbed and some not (Bodet et al., 2008). Ellagic acid was absorbed in a short time, but not chlorogenic acid; this behavior may be due to absorption of ellagic acid in the upper part of the gut, in the stomach and small intestine. Chlorogenic acid is a caffeic acid ester linked to quinic acid, and there are no esterases in human tissues able to hydrolyze chlorogenic acid. According to this, small intestine of rats metabolizes only a very small amount of chlorogenic acid. In the same way, colonic microflora is the only available site for chlorogenic acid metabolism (Aiyer et al., 2008). 8. Effect of processing conditions on bioactive compounds characteristics The antioxidative and antimicrobial activities depend on the cultivar, growth conditions, and storage of raw material. The composition of pigments may also differ depending on the plant cultivar and agroclimatic growth conditions and the method of extraction of bioactive compounds (Viskelis et al., 2009). Some anthocyanins are more stable than others depending on their molecular structure, malvidin glycosides stability relies on dimethyloxilation reactions in most cases (Nikkhah, Khayamy, Heidari, & Jamee, 2007). The stability of anthocyanin pigments is dependent on various factors including structure, concentration, pH, temperature, light intensity, and presence of other pigments along with metal ions, enzymes, oxygen, ascorbic acid, sugars and sugars derivatives, etc. (Mazza & Manitiati, 1993, chap. 1). Sucrose protects anthocyanins from degrading during processing and storage. Sucrose concentration of 20% has protective effect on anthocyanins structure, but in higher concentration this effect is decreased (Nikkhah et al., 2007). Processing methods varying in the number of steps and conditions such as temperature, pressure and time can markedly affect the anthocyanin content and antioxidant capacity of berries (Brownmiller et al., 2008). Several studies have investigated the effects of processing steps on berry anthocyanins. Freezing and subsequent frozen storage have shown to have minimal effects on red raspberry anthocyanins (Mullen et al., 2002). However, significant losses of anthocyanins have been observed in blueberry juices (Srivastava, Akoh, Yi, Fischer, & Krewer, 2007), raspberry puree (Ochoa, Kesseler, Vullioud, & Lozano, 1999), and strawberry jams (Ngo, Wrolstad, & Zhao, 2007), juice and nectar (Klopotek, Otto, & Böhm, 2005). Michalczyk, Macura, and Matuszak (2009) demonstrated that even after long-term storage and despite exposure to atmospheric oxygen, freeze-dried berries retain the antioxidant properties of the raw material in a high level. Therefore, lyophilisates can satisfy this particular requirement. Air-dried berries are less stable during long-term storage (Kwok, Hu, Durance, & Kitts, 2004). High hydrostatic pressure (HHP) processing offers the possibility to preserve berry products while affecting their chemical components less than heat pasteurization. Changes could appear in the composition of flavor compounds after HHP treatment at 800 MPa, or after heat sterilization. However, lower pressure or thermal levels are sufficient to pasteurize berry products (Dalmadi, Lara, & O'Hill, 2006). Strawberries stored at high oxygen atmospheres showed higher antioxidant capacity, higher total phenolics, less decay, and longer postharvest life than those stored at normal air composition, also the production of some volatile compounds such as methyl acetate and methyl hexanoate is increased (Ayala-Zavala et al., 2007). Han et al. (2007) evaluated polyphenol retention, total polyphenols concentration, anthocyanin content, and antioxidant activity in blueberries dried by means of combining microwave-vacuum, hot-air drying and freeze drying technologies. Ellagic acid, quercetin, and kaempferol exhibited a higher retention than phloridizin, and R- and S-naringin in
dried blueberries following a dehydration process. With this technology dried blueberries had a higher retention of polyphenols and anthocyanins, and therefore a higher antioxidant activity. The possibility of phenolic compound retention in blackberries due to sugar addition during cold storage has been investigated. Results showed that glucose had positive effects on anthocyanin retention as well as total phenolic compound content, an important conclusion of this was that the higher retention of phenolic compounds the more effective against oxidative stress in human body (Kopjar et al., 2009). There is an important lack of information about the effect of different processing methods and long-term storage on nutritional quality of berry-products prepared from the same raw material. This information is important for consumers who wish to incorporate higher levels of bioactive compounds into their diet via berries consumption and the industry which desires to retain or possibly improve levels of bioactive compounds in their products (Michalczyk et al., 2009).
9. Metabolomic engineering of berry bioactive compounds The economic value of bioactive compounds has encouraged many researchers to study secondary metabolite profiles in ripe berries, with GC–MS used to analyze volatiles and LC–MS used to analyze non-volatiles. Most studies in the latter category have focused on one or a small group of related compounds, such as anthocyanins (Toffali et al., 2011; Wang, Race, & Shrikhande, 2003), procyanidins (Wu, Wang, & Simon, 2005), or anthocyanins and flavonols (Downey & Rochfort, 2008; Mattivi, Guzzon, Vrhovsek, Stefanini, & Velasco, 2006). A small number of more comprehensive studies have been reported, including one encompassing anthocyanins, flavonols and hydroxycinnamic acids (Guerrero, Liazid, & Palma, 2009) and other covering anthocyanins, procyanidins, flavonols and stilbenes (Cavaliere et al., 2008; Toffali et al., 2011). The latter are probably the broadest investigations carried out thus far, involving the simultaneous detection of 40 different compounds in the berry skins of three different table cultivars. Although the static metabolic profiles of ripe berries have received the greatest attention, less studies have looked at how metabolic profiles change during development and ripening. A complete qualitative–quantitative investigation has been performed on stilbene and viniferin profiles (Gatto et al., 2008) and volatile compounds in berrycactus (Vazquez-Cruz et al., 2012). Recently, the holistic analysis of metabolic profiles during berry development and ripening has become possible through the use of software that can extract the maximum amount of information from chromatograms (Toffali et al., 2011). This software uses different algorithms to perform three main tasks: signal/molecule recognition over noise; alignment of retention times for specific compounds across multiple chromatograms, and building of a data matrix suitable for statistical analysis. It has been recently reported a systems biology analysis of the Italian cultivar Corvina, which is used fresh from the vine to produce wines such as Bardolino and Valpolicella, and also after withering (a post-harvest drying process) for the production of fine wines such as Recioto and Amarone (Stewart, McDougall, et al., 2007; Stewart, Stankovic, et al., 2007; Zamboni, Di Carli, & Guzzo, 2010). The study showed that the berry transcriptome undergoes extensive reprogramming during withering, whereas the metabolome changes most significantly passing through veraison (the onset of ripening). Moreover, the integration of the metabolite, protein and transcript datasets in hypothesis-free and hypothesis-driven approaches showed that various metabolites, such as coumarated anthocyanins, flavanones and stilbenes, which are accumulated mainly during withering, correlated with stress and pathogenesisinduced transcripts and proteins (Stewart, McDougall, et al., 2007; Stewart, Stankovic, et al., 2007; Toffali et al., 2011).
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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10. Quality trait locus related to bioactive compounds production in berries In the past decade, research on plant quantitative trait loci (QTL) has successfully identified numerous loci controlling the genetic variation of complex traits in plants. Price (2006) reported 30 studies of successful QTL cloning concerning nine plant species, but these researches have been conducted only in biparental populations, revealing only a slice of the genetic architecture for the trait (Fournier-Level et al., 2009; Holland, 2007). The widespread availability of plant genomic and genetic resources has triggered the need for more integrated research (Fanniza, Lamaj, Constantini, Chaabane, & Grando, 2005; Flint-Garcia, Thuillet, Yu, Pressoir, & Romero, 2005) that is likely to combine the findings of different approaches from various experimental designs, as it has already been done for humans (Hirschhorn & Daly, 2005), animals (Ron & Weller, 2007), and plants (Aranzana, Kim, Zhao, Bakker, & Horton, 2005; McCallum et al., 2010; Osterberg, Shavorskaya, Lascoux, & Lagercrantz, 2002). The number of grape genomic resources has increased considerably over the past few years and the sequencing of the grape genome has recently been completed (Fouenier-Level et al., 2011; Jaillon, Aury, Noel, Policriti, & Clepet, 2007; Velasco, Zharkikh, Troggio, Cartwright, & Cestaro, 2007). Taking advantage of these new resources considerable progress will be able in complex trait dissection, given that the access to candidate genes is straightforward, and will allow the cloning of QTL. Grape shows extended genetic variations with a high level of linkage disequilibrium (LD) (Barnaud, Lacombe, & Doligez, 2006) that makes a genetic association strategy feasible, as it has already been performed in model plants (Flint-Garcia et al., 2005) or other perennial plants (Brennan & Graham, 2009; Gonzalez-Martinez, Wheeler, Ersoz, Nelson, & Neale, 2007). A reference mapping population has been developed in raspberry and replicated within and across different sites (Graham et al., 2004). This population is being utilized to map QTLs for various quality traits. Increasingly QTL resources have been used to develop functional gene-based markers (Woodhead et al., 2008), through a more knowledge-based approach linking genes to markers. QTLs describing the overall fruit ripening process have been located using summary statistics derived from scoring the stages of ripening in both field and protected growing environments across different seasons (Graham, Ratnaparkhe, & Powell, 2008). Interestingly gene H on chromosome 2 (Graham, Smith, Tierney, Mackenzie, & Hackett, 2006) is known to determine cane pubescence but is also associated with a slowing down of ripening across all stages from open flowers to the green/red fruit. Hairs and spines are both outgrowths of epidermal cells and their early development is inter-related (Graham et al., 2008). It would therefore seem likely that gene H acts early in development and has been postulated to delay cell maturity. Chromosome 3 had a strong effect on ripening with a broad range of significant markers identified suggesting that more than one QTL is involved (McCallum et al., 2010). Many important agronomic traits are quantitatively inherited and thus difficult their control in grapevine breeding. The elucidation of inheritance of complex characteristics can be addressed by establishing their association with linked molecular markers. Genetic factors involved in the variation of traits can be localized as quantitative trait loci (QTL) on the basis of a molecular map introduced into plant genetics by Paterson et al. (1988) and later modified into QTL interval mapping (Lander & Botstein, 1989). Thus, the first grape mapping studies started on populations comprising between 50 and 80 individuals (Zheng & Hrazdina, 2008), involving American genotypes such as ‘Cayuga White’ and ‘Aurore’ (McCallum et al., 2010), wild species native to China (Luo et al., 2008) and other varieties such as seedlessness grapes (Doligez et al., 2002). Some investigations have been focused on identifying resistance-correlated factors in Vitis ssp. (Fournier-Level et al., 2009). In order to create a segregating population of 153F1 individuals for mapping, the new fungus-resistant variety ‘Regent’ was crossed to the fungus-susceptible, traditional red wine cultivar ‘Lemberger’ (Ambrosi,
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Detteweiler-Munch, Rohl, Schmid, & Schumann, 1998). The progeny were genotyped with a variety of dominant [random amplified polymorphic DNA [RAPD], amplified fragment length polymorphism (AFLP), sequence characterized amplified region (SCAR)], and co-dominant [single sequence repeat (SSR)] markers. Genetic maps of both parental types were developed separately by linkage and recombination analysis following the double pseudo-test-cross strategy and aligned to each other and integrated into consensus linkage groups. The individuals were phenotypically investigated for their resistance levels to P. viticola and U. necator, as well as some additional agronomic traits in the field (McCallum et al., 2010). The addition of all this new information about the genetics of an ancient cultured plant will allow comparisons within grapevine varieties and accelerate the overall understanding of the physiological basis of quality traits desired in modern grapevine breeding. In addition to quantitative fungus resistances, QTLs for traits such as the tendency of axillary shoot growth, berry size and the beginning of ripening. Another detailed QTL analysis for quantitative traits different from pathogen resistance in grape has so far only been reported for the characteristics of seedless grapes and berry weight as important traits for table grape breeding (Doligez et al., 2002). 11. Future challenges There should be a strong emphasis on the interdisciplinary character of berry research conducted through the basic and clinical sciences point of view. The role of berry phytochemicals in human health and disease, is an important gaps in our knowledge concerning the biology and chemistry of these compounds (Stewart, McDougall, et al., 2007; Stewart, Stankovic, et al., 2007). Future studies should be designed to enhance our knowledge of the intricate roles and functions that berry phytochemicals exert at both cellular and molecular levels. In addition, the research progress about the potential health benefits of berries continue in a post-genomic era, as a consequence it will bring everincreasing demands to observe and characterize variations within biological systems. Research focusing on nutrigenomics (effects of nutrients on the genome, proteome, and metabolomics) and nutrigenetics (effects of genetic variation on the interaction between diet and disease) will be essential (Hall, Nauhauser, & Cotner, 2008). Future studies on metabolomics of bioactive compounds in berry are necessary, and there should be renewed on evaluating strategies whether metabolites formed in vivo accumulate within target tissues and exert biological effects therein. For example, it may be possible that on ingestion, metabolites including glucuronidated, sulfated, and methylated derivatives may act as “pro-drugs” within target tissue sites (Shukla & Matto, 2009). In addition, the products formed from the action of colonic microflora on berry phenolics may also significantly contribute to health benefits that may result from berry consumption (Stewart, McDougall, et al., 2007; Stewart, Stankovic, et al., 2007). Studies should also be conducted to evaluate if biological effects of berry phytochemicals are enhanced by complex interactions of multiple components within the food matrix of a particular fruit compared to a single purified constituent or constituents. In addition, health benefits of berry fruits enhanced through additive and/or synergistic interactions with phytochemicals from other foods should be examined. Future berry research should also been focused on studying gene-nutrient interactions and health outcomes to achieve individual dietary intervention strategies directed to prevent human chronic diseases, improving life, and promoting healthy aging. 12. Conclusions The accumulated research experience, knowledge and practical methodology applications during the last years concerning bioactive berry compounds, in particular phenolic compounds, flavonoids, anthocyanin, tannins and phenolic compounds have increased a lot. It seems that research efforts will pay special attention on bioavailability of
Please cite this article as: Jimenez-Garcia, S.N., et al., Functional properties and quality characteristics of bioactive compounds in berries: Biochemistry, biotechnology, and genomics, Food Research International (2012), http://dx.doi.org/10.1016/j.foodres.2012.11.004
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antioxidant compounds and chronic degenerative diseases prevention. The biosynthetic capacity of plants in relation to their secondary metabolites should be evaluated in a more careful way, especially concerning their outstanding functional potential. The utilization of antimicrobial activity of berry bioactive compounds as natural antimicrobial agents offers many opportunities for their use in food industry and medicine. It is also pertinent to emphasize plant breeding and genetic approaches in relation with the synthesis of compounds for nutrition and health purposes should receive more emphasis and attention. If research can be applied to enhance plant-derived food functional properties in a feasible period of time and within the current economic conditions, every opportunity must be taken to ensure that we are taking the optimum level of information regarding knowledge about nutritional properties of berry compounds. The next step would be to develop markerassisted breeding approaches based on mapping robust data derived from well-replicated field trials over different environments.
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