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Abstract
The post-harvest processing of strawberries generates considerable amounts of by-products that consist of the inedible parts of the fruit (sepal, calyx, stem, and non-marketable portion of the fruit), which is an environmental problem for local producers and industries. This study aimed to revalue these kinds of tissues through identifying and quantifying the genotype influence on the total phenolic content, phenolic profile, and the antioxidant activity of the by-products from three strawberry cultivars: ‘Festival’ (FE), ‘San Andreas ‘ (SA), and ‘Camino Real’ (CR). The total phenolic content was determined by the Folin–Ciocalteu method, in-vitro antioxidant activity by the DPPH* radical scavenging method and the phenolic profile by PAD–HPLC. The different genotypes showed significant differences (p < 0.05) in total phenolic content (TPC), FE being the one with the highest TPC (14.97 g of gallic acid equivalents < GAE > /Kg of by-product < R >), followed by SA and CR cultivars. The antioxidant capacity of the SA and FE tissues were similar (p > 0.05) and higher (15.1–16.3 mmol Trolox equivalents < TE > /Kg R) than CR. Eight main phenolic compounds were identified and quantified on the three cultivars. Agrimoniin was the principal polyphenol (0.38–1.56 g/Kg R), and the cultivar FE had the highest concentration. This compound showed the highest correlation coefficient with the antioxidant capacity (R 2 0.87; p < 0.001). This study highlighted the impact of the multi-cultivar systems in strawberry production on the bioactive potential and the diversity of secondary metabolites obtained from strawberry agro-industrial by-products at a low cost.
Keywords
Agro-industrial by-products
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Strawberry cultivars
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Revalorisation
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Bioactive compounds
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Hydrolysable tannins
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Antioxidants
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Esteban Villamil-Galindo, Franco Van de Velde, Andrea M. Piagentini.
Strawberry agro-industrial by-products as a source of bioactive compounds: effect of cultivar on the phenolic profile and the antioxidant capacity.
Bioresources and Bioprocessing, 2021, 8(1): 61 DOI:10.1186/s40643-021-00416-z
| [1] |
Aaby K, Mazur S, Nes A, Skrede G. Phenolic compounds in strawberry (Fragaria × ananassa Duch.) fruits: composition in 27 cultivars and changes during ripening. Food Chem, 2012, 132(1): 86-97.
|
| [2] |
Aguayo RDC, Yahia EM. Correlation between some nutritional components and the total antioxidant capacity measured with six different assays in eight horticultural crops. J Agric Food Chem, 2008, 56: 10498-10504.
|
| [3] |
Alfei S, Turrini F, Catena S, Zunin P, Grilli M, Pittaluga AM, Boggia R. Ellagic acid a multi-target bioactive compound for drug discovery in CNS? A narrative review. Eur J Med Chem, 2019, 183: 111724.
|
| [4] |
Aryal S, Baniya M, Danekhu K, Kunwar P, Gurung R, Koirala N. Total phenolic content, flavonoid content and antioxidant potential of wild vegetables from western Nepal. Plants, 2019, 8: 96.
|
| [5] |
Axel E (2016) Cultivos anuales y bianuales de frutilla en el Sudeste de la provincia de Buenos Aires: Modificaciones en los parámetros de crecimiento [Universidad Nacional del Litoral]. http://hdl.handle.net/11185/851
|
| [6] |
Basu A, Nguyen A, Betts NM, Lyons TJ. Strawberry as a functional food: an evidence-based review. Crit Rev Food Sci Nutr, 2014, 54(6): 790-806.
|
| [7] |
Buendía B, Gil MI, Tudela JA, Gady AL, Medina JJ, Soria C, López JM, Tomás-Barberán FA. HPLC-MS analysis of proanthocyanidin oligomers and other phenolics in 15 strawberry cultivars. J Agric Food Chem, 2010, 58(7): 3916-3926.
|
| [8] |
Connor A, Luby J, Tong C, Finn C, Hancock J. Genotypic and environmental variation in antioxidant activity, total phenolic content, and anthocyanin content among blueberry cultivars. J Am Soc Horticult Sci, 2002, 127: 89-97.
|
| [9] |
Di Vittori L, Mazzoni L, Battino M, Mezzetti B. Pre-harvest factors influencing the quality of berries. Sci Horticult, 2018, 233: 310-322.
|
| [10] |
Fotirić Akšić M, Dabić Zagorac D, Sredojević M, Milivojević J, Gašić U, Meland M, Natić M. Chemometric characterization of strawberries and blueberries according to their phenolic profile: combined effect of cultivar and cultivation system. Molecules (basel, Switzerland), 2019, 24(23): 1-25.
|
| [11] |
Francini A, Giro A, Ferrante A (2019) Biochemical and molecular regulation of phenylpropanoids pathway under abiotic stresses. In: Plant signaling molecules: role and regulation under stressful environments. Elsevier Inc. https://doi.org/10.1016/B978-0-12-816451-8.00011-3
|
| [12] |
Girotto F, Alibardi L, Cossu R. Food waste generation and industrial uses: a review. Waste Manage, 2015, 45: 32-41.
|
| [13] |
González-Barrio R, Borges G, Mullen W, Crozier A. Bioavailability of anthocyanins and ellagitannins following consumption of raspberries by healthy humans and subjects with an ileostomy. J Agric Food Chem, 2010, 58(7): 3933-3939.
|
| [14] |
Grochowski DM, Skalicka-Woźniak K, Orhan IE, Xiao J, Locatelli M, Piwowarski JP, Granica S, Tomczyk M. A comprehensive review of agrimoniin. Ann N Y Acad Sci, 2017, 1401(1): 166-180.
|
| [15] |
Gündüz K (2015) Strawberry: phytochemical composition of strawberry (Fragaria × ananassa). In: Nutritional composition of fruit cultivars. Elsevier Inc. https://doi.org/10.1016/B978-0-12-408117-8.00030-1
|
| [16] |
Halbwirth H, Puhl I, Haas U, Jezik K, Treutter D, Stich K. Two-phase flavonoid formation in developing strawberry (Fragaria × ananassa) fruit. J Agric Food Chem, 2006, 54(4): 1479-1485.
|
| [17] |
Hoffmann J, Casetti F, Bullerkotte U, Haarhaus B, Vagedes J, Schempp CM, Wölfle U. Anti-inflammatory effects of agrimoniin-enriched fractions of Potentilla erecta. Molecules, 2016, 21(6): 792.
|
| [18] |
Ibanez F, Bang WY, Lombardini L, Cisneros-Zevallos L. Solving the controversy of healthier organic fruit: Leaf wounding triggers distant gene expression response of polyphenol biosynthesis in strawberry fruit (Fragaria × ananassa). Sci Rep, 2019, 9(1): 1-11.
|
| [19] |
Jacobo-Velázquez DA, Cisneros-Zevallos L. Bioactive phenolics and polyphenols: current advances and future trends. Int J Mol Sci, 2020, 21(17): 1-4.
|
| [20] |
Kaderides K, Mourtzinos I, Goula AM. Stability of pomegranate peel polyphenols encapsulated in orange juice industry by-product and their incorporation in cookies. Food Chem, 2020, 310: 125849.
|
| [21] |
Karlińska E, Masny A, Cieślak M, Macierzyński J, Pecio Ł, Stochmal A, Kosmala M. Ellagitannins in roots, leaves, and fruits of strawberry (Fragaria × ananassa Duch.) vary with developmental stage and cultivar. Sci Hortic, 2021, 275: 109665.
|
| [22] |
Kårlund A, Salminen J-P, Koskinen P, Ahern J, Karonen M, Tiilikkala K, Karjalainen R. Polyphenols in strawberry (Fragaria × ananassa ) leaves induced by plant activators. J Agric Food Chem, 2014, 62: 4592-4600.
|
| [23] |
Kashchenko NI, Chirikova NK, Olennikov DN. Agrimoniin, an active ellagitannin from comarum palustre herb with anti-α-glucosidase and antidiabetic potential in streptozotocin-induced diabetic rats. Molecules, 2017, 22(1): 73.
|
| [24] |
Kelly KE (2018) Synthesis, oxidation , and distribution of polyphenols in strawberry fruit during cold storage by (Issue June) [University of South Florida]. https://scholarcommons.usf.edu/etd
|
| [25] |
Landete JM. Ellagitannins, ellagic acid and their derived metabolites: a review about source, metabolism, functions and health. Food Res Int, 2011, 44(5): 1150-1160.
|
| [26] |
Mazur SP, Aaby K, Mazur S, Nes A, Skrede G. Phenolic compounds in strawberry ( Fragaria × ananassa Duch.) fruits: composition in 27 cultivars and changes during ripening Phenolic compounds in strawberry ( Fragaria x ananassa Duch.) fruits: Composition in 27 cultivars and changes during ripening. Food Chem, 2012, 132(1): 86-97.
|
| [27] |
Mikkonen TP, Hukkanen AT, Määttä KR, Kokko HI, Törrönen AR, Kärenlampi SO, Karjalainen RO. Flavonoid content in strawberry cultivars. Acta Hortic, 2002, 567: 815-818.
|
| [28] |
Moilanen J, Koskinen P, Salminen JP. Distribution and content of ellagitannins in finnish plant species. Phytochemistry, 2015, 116(1): 188-197.
|
| [29] |
Morales-Quintana L, Ramos P. Chilean strawberry (Fragaria chiloensis): an integrative and comprehensive review. Food Res Int, 2019, 119: 769-776.
|
| [30] |
Muñoz C, Sánchez-Sevilla JF, Botella MA, Hoffmann T, Schwab W, Valpuesta V. Polyphenol composition in the ripe fruits of fragaria species and transcriptional analyses of key genes in the pathway. J Agric Food Chem, 2011, 59(23): 12598-12604.
|
| [31] |
Nowicka A, Kucharska AZ, Sokół-Łętowska A, Fecka I. Comparison of polyphenol content and antioxidant capacity of strawberry fruit from 90 cultivars of Fragaria × ananassa Duch. Food Chem, 2019, 270: 32-46.
|
| [32] |
Pinelide LO, Moretti CL, Dos Santos MS, Campos AB, Brasileiro AV, Córdova AC, Chiarello MD. Antioxidants and other chemical and physical characteristics of two strawberry cultivars at different ripeness stages. J Food Composition Anal, 2011, 24(1): 11-16.
|
| [33] |
Przybylska D, Kucharska AZ, Cybulska I, Sozański T, Piórecki N, Fecka I. Cornus mas L. Stones: a valuable by-product as an ellagitannin source with high antioxidant potential. Molecules (basel, Switzerland), 2020, 25(20): 4646.
|
| [34] |
Raudsepp P, Kaldmäe H, Kikas A, Libek AV, Püssa T. Nutritional quality of berries and bioactive compounds in the leaves of black currant (Ribes nigrum L.) cultivars evaluated in Estonia. J Berry Res, 2010, 1(1): 53-59.
|
| [35] |
Ravindran R, Hassan SS, Williams GA, Jaiswal AK. A review on bioconversion of agro-industrial wastes to industrially important enzymes. Bioengineering, 2018, 5(4): 1-20.
|
| [36] |
Rodríguez-Arzuaga M, Salsi MS, Piagentini AM. Storage quality of fresh-cut apples treated with yerba mate (Ilex paraguariensis). J Food Sci Technol, 2021, 58(1): 186-196.
|
| [37] |
Simirgiotis MJ, Theoduloz C, Caligari PDS, Schmeda-Hirschmann G. Comparison of phenolic composition and antioxidant properties of two native Chilean and one domestic strawberry genotypes. Food Chem, 2009, 113(2): 377-385.
|
| [38] |
Sordo M, Travadelo M, Pernuzzi C (2017) Evolución del cultivo de frutilla en la provincia de Santa Fe (Argentina) en los últimos 50 años. Hortintl Cals Ncsu Edu 36(90): 13–24. https://hortintl.cals.ncsu.edu/sites/default/files/documents/2017decemberevoluciondelcultivodefrutillaenlaprovinciadesantafeargentinaenlosultimos50anos.pdf
|
| [39] |
Tulipani S, Mezzetti B, Capocasa F, Bompadre S, Beekwilder J, De Vos R, Capanoglu E, Bovy A, Battino M. Antioxidants, phenolic compounds, and nutritional quality of different strawberry genotypes. J Agric Food Chem, 2008, 56: 696-704.
|
| [40] |
Valentinuzzi F, Mason M, Scampicchio M, Andreotti C, Cesco S, Mimmo T. Enhancement of the bioactive compound content in strawberry fruits grown under iron and phosphorus deficiency. J Sci Food Agric, 2015, 95(10): 2088-2094.
|
| [41] |
Van De Velde F, Tarola A, Güemes D, Pirovani M. Bioactive compounds and antioxidant capacity of camarosa and selva strawberries (Fragaria × ananassa Duch.). Foods, 2013, 2(2): 120-131.
|
| [42] |
Van de Velde F, Grace MH, Pirovani MT, Lila MA (2016) Impact of a new postharvest disinfection method based on peracetic acid fogging on the phenolic profile of strawberries. Postharvest Biol Technol 117. https://doi.org/10.1016/j.postharvbio.2016.03.005
|
| [43] |
Van de Velde F, Esposito D, Grace MH, Pirovani ME, Lila MA. Anti-inflammatory and wound healing properties of polyphenolic extracts from strawberry and blackberry fruits. Food Res Int, 2019, 121: 453-462.
|
| [44] |
Vauchel P, Colli C, Pradal D, Philippot M, Decossin S, Dhulster P, Dimitrov K. Comparative LCA of ultrasound-assisted extraction of polyphenols from chicory grounds under different operational conditions. J Clean Prod, 2018, 196: 1116-1123.
|
| [45] |
Villamil-Galindo E, Van de Velde F, Piagentini AM. Extracts from strawberry by-products rich in phenolic compounds reduce the activity of apple polyphenol oxidase. Lwt, 2020, 133.
|
| [46] |
Wang SY, Camp MJ. Temperatures after bloom affect plant growth and fruit quality of strawberry. Sci Hortic, 2000, 85(3): 183-199.
|
| [47] |
Wang BQ, Jin ZX. Agrimoniin induced SGC7901 cell apoptosis associated mitochondrial transmembrane potential and intracellular calcium concentration. J Med Plants Res, 2011, 5(15): 3513-3519.
|
| [48] |
Welti-Chanes J, Morales-de la Peña M, Jacobo-Velázquez DA, Martín-Belloso O. Opportunities and challenges of ultrasound for food processing: an industry point of view. Ultrasound Adv Food Process Preserv, 2017
|
| [49] |
Zhu Q, Nakagawa T, Kishikawa A, Ohnuki K, Shimizu K. In vitro bioactivities and phytochemical profile of various parts of the strawberry (Fragaria × ananassa var. Amaou). J Funct Foods, 2015, 13: 38-49.
|
| [50] |
Zielinski AAF, Haminiuk CWI, Beta T. Multi-response optimization of phenolic antioxidants from white tea (Camellia sinensis L. Kuntze) and their identification by LC-DAD-Q-TOF-MS/MS. LWT Food Sci Technol, 2016, 65: 897-907.
|
Funding
Agencia Nacional de Promoción Científica y Tecnológica(PICT 2017-406)