Changes in phenolic compounds and antioxidant capacity of Andean raspberries in response to Peronospora sparsa
Published
Aug 18, 2020
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Nathalia Cardona-Hurtado
https://orcid.org/0000-0002-3814-4726
Gloria E Guerrero-Alvarez
https://orcid.org/0000-0002-0529-5835
Ana M López-Gutiérrez
https://orcid.org/0000-0002-5138-1806
https://orcid.org/0000-0002-3814-4726
Gloria E Guerrero-Alvarez
https://orcid.org/0000-0002-0529-5835
Ana M López-Gutiérrez
https://orcid.org/0000-0002-5138-1806
##plugins.themes.bootstrap3.article.details##
Abstract
In Colombia, the Andean raspberry (Rubus glaucus Benth) is of large economic significance because of its use in industry and widespread consumption as a fresh fruit. However, this crop is highly susceptible to disease by Peronospora sparsa, a fungus that causes between 50 % and 70 % production loss. Plants respond to pathogen-induced damage by increasing the production of specific secondary metabolites, such as phenolic compounds, which have broad industrial applications. This work estimated the antioxidant capacity and phenolic content of healthy and Peronospora sparsa-infected Andean raspberry fruits. Antioxidant capacity was analyzed by DPPH and FRAP methods, while phenolic compounds were analyzed by high performance liquid chromatography coupled to diode array detection (HPLC-DAD). According to the DPPH method, antioxidant capacity increased from 45.9 ± 1.61 µmol TE g−1 fresh sample in healthy fruits to 67.02 ± 0.58 µmol TE g−1 fresh sample in affected fruits. The FRAP method revealed an antioxidant response difference from 5.19 ± 0.8 mmol TE 100 g−1 fresh sample in healthy fruits vs. 10.97 ± 0.27 mmol TE 100 g−1 fresh sample in affected fruits. The phenolic compound content was observed in a range of 4.14 ± 1.16 to 72.03 ± 26.68 mg GAE L−1 for healthy fruits and from 4.48 ± 1.76 to 221.89 ± 1.18 mg GAE L−1 for affected fruits. Phenolic acids were the main phenols detected, encompassing derivatives of gallic acid, chlorogenic acid, ferulic acid, ellagic acid, and p-coumaric acid. This work confirmed that the Peronospora sparsa-infected berries contained relatively more antioxidants and phenolic acid compounds than their healthy counterparts, and that this difference was likely due to a defense mechanism to cope with pathogen-induced damage.
Keywords
antioxidants, liquid chromatography, pathogens, phenolic acids, Rubus glaucus Benth
References
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doi: 10.1515/JPPR-2017-0043
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doi: 10.1111/1750-3841.12148
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doi: 10.1021/jf071475d
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doi: 10.1016/j.foodchem.2011.12.026
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doi: 10.15446/rfna.v70n2.64521
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doi: 10.1007/s10658-017-1232-7
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doi: 10.1590/0034-737x201966010002
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doi: 10.5154/r.rchsh.2014.02.010
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[17] Guzmán-Nieves CA. Proceso de obtención de un extracto de compuestos fenólicos a partir de orujo de uva tinta Vitis vinifera a bajas temperaturas para aplicación en alimentos y bebidas destinados a consumo humano y animal, México, WO2011062468A2, clasificación A23L33/105, 24 de junio 2011.
https://patents.google.com/patent/WO2011062468A2/es
[18] Velićanski AS, Cvetković DD, Markov SL. Screening of antibacterial activity of raspberry (Rubus idaeus L.) fruit and pomace extracts. Acta Periodica Technologica, 43 (43): 305-313, 2012.
doi: 10.2298/APT1243305V
[19] Abu-Bakar MF, Ismail NA, Isha A, Mei-Ling AL. Phytochemical composition and biological activities of selected wild berries (Rubus moluccanus L., R. fraxinifolius Poir, and R. alpestris Blume). Evidence-Based Complementary and Alternative Medicine, 2016: 110, 2016.
doi: 10.1155/2016/2482930
[20] Guerrero G, Suarez M, Moreno G. Derivados hidroxicinámicos para la discriminación de genotipos de café. Cenicafé, 54 (3): 234- 241, 2004.
[21] Calderón-Oliver M, Escalona-Buendía HB, Medina-Campos ON, Pedraza-Chaverri J, Pedroza-Islas R, Ponce Alquicira E. Optimization of the antioxidant and antimicrobial response of the combined effect of nisin and avocado byproducts. LWT -Food Science and Technology, 65: 46-52, 2016.
doi: 10.1016/j.lwt.2015.07.048
[22] Estupiñan DC, Schwartz SJ, Garzón GA. Antioxidant activity, total phenolics content, anthocyanin, and color stability of isotonic model beverages colored with Andes Berry (Rubus glaucus Benth) anthocyanin powder. Journal of Food Science, 76 (1): S26-S34, 2011.
doi: 10.1111/j.1750-3841.2010.01935.x
[23] Fontaine BM, Nelson K, Lyles JT, Jariwala PB, GarcíaRodriguez JM, Quave CL, Weinert EE. Identification of ellagic acid rhamnoside as a bioactive component of a complex botanical extract with anti-biofilm activity. Frontiers in Microbiology, 8(MAR): 496, 2017.
doi: 10.3389/fmicb.2017.00496
[24] Balasundram N, Sundram K, Samman S. Phenolic compounds in plants and agro-industrial by-products: Antioxidant activity, occurrence, and potential uses. Food Chemistry, 99 (1): 191-203, 2006.
doi: 10.1016/j.foodchem.2005.07.042
[25] Sharma OP, Bhat TK. DPPH antioxidant assay revisited. Food Chemistry, 113 (4): 1202-1205, 2009.
doi: 10.1016/j.foodchem.2008.08.008
[26] Prior RL, Wu X, Schaich K. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. Journal of Agricultural and Food Chemistry, 53 (10): 4290-4302, 2005.
doi: 10.1021/jf0502698
[27] Jones A, Pravadali-Cekic S, Dennis GR, Bashir R, Mahon PJ, Shalliker RA. Ferric reducing antioxidant potential (FRAP) of antioxidants using reaction flow chromatography. Analytica Chimica Acta, 967: 93-101, 2017.
doi: 10.1016/J.ACA.2017.02.032
[28] Vasco C, Ruales J, Kamal-Eldin A. Total phenolic compounds and antioxidant capacities of major fruits from Ecuador. Food Chemistry, 111 (4): 816-823, 2008.
doi: 10.1016/j.foodchem.2008.04.054
[29] Bernal LJ, Melo LA, Díaz Moreno C. Evaluation of the antioxidant properties and aromatic profile during maturation of the blackberry (Rubus glaucus Benth) and the bilberry (Vaccinium meridionale Swartz). Revista Facultad Nacional de Agronomía, 67 (1): 7209-7218, 2014.
doi: 10.15446/rfnam. v67n1.42649
[30] Wang SY, Lin HS. Antioxidant activity in fruits and leaves of blackberry, raspberry, and strawberry varies with cultivar and developmental stage. Journal of Agricultural and Food Chemistry, 48 (2): 140-146, 2000.
doi: 10.1021 / jf9908345
[31] Sellappan S, Akoh CC, Krewer G. Phenolic compounds and antioxidant capacity of Georgia-grown blueberries and blackberries. Journal of Agricultural and Food Chemistry, 50 (8): 2432-2438, 2002.
doi: 10.1021/jf011097r
[32] Garzón G, Riedl K., Schwartz S. Determination of anthocyanins, total phenolic content, and antioxidant activity in Andes berry (Rubus glaucus Benth). Food Science, 74 (3): C227-C232, 2009.
doi: 10.1111/j.1750-3841.2009.01092.x
[33] Zacarés L, López-Gresa MP, Fayos J, Primo J, Bellés JM, Conejero V. Induction of p-coumaroyldopamine and feruloyldopamine, two novel metabolites, in tomato by the bacterial pathogen Pseudomonas syringae. Molecular Plant-Microbe Interactions, 20 (11): 1439-1448, 2007.
doi: 10.1094/MPMI-20-11-1439
[34] Ribera A, Zuñiga G. Induced plant secondary metabolites for phytopathogenic fungi control: A review. Journal of Soil Science and Plant Nutrition, 12 (4): 893-911, 2012.
doi: 10.4067/S0718-95162012005000040
[35] Mikulic-Petkovsek M, Schmitzer V, Stampar F, Veberic R, Koron D. Changes in phenolic content induced by infection with Didymella applanata and Leptosphaeria coniothyrium, the causal agents of raspberry spur and cane blight. Plant Pathology, 63(1): 185-192, 2014.
doi: 10.1111/ppa.12081
[36] Badhani B, Sharma N, Kakkar R. Gallic acid: a versatile antioxidant with promising therapeutic and industrial applications. RSC Advances, 5 (35): 27540-27557, 2015.
doi: 10.1039/C5RA01911G
[37] Do QD, Angkawijaya AE, Tran-Nguyen PL, Huynh LH, Soetaredjo FE, Ismadji S, Ju YH. Effect of extraction solvent on total phenol content, total flavonoid content, and antioxidant activity of Limnophila aromatica. Journal of Food and Drug Analysis, 22 (3): 296-302, 2014.
doi: 10.1016/J.JFDA.2013.11.001
[38] Carbonel KN, Suárez-Cunza S, Arnao I. Características fisicoquímicas y capacidad antioxidante in vitro del extracto de Gentianella nitida. Anales de la Facultad de Medicina, 77 (4): 333-337, 2016.
doi: 10.15381/anales. v77i4.12648
[39] Paredes-López O, Cervantes-Ceja ML, Vigna-Pérez M, Hernández-Pérez T. Berries: Improving human health and healthy aging and promoting quality life—A Review. Plant Foods for Human Nutrition, 65 (3): 299-308, 2010.
doi: 10.1007/s11130-010-0177-1
doi: 10.3390/foods5040088
[2] Farahani AS, Taghavi M. Effects of bacterial populations, temperature, and exogenous hydrogen peroxide on the induction of the hypersensitive response in Nicotiana tabacum against Xanthomonas perforans. Journal of Plant Protection Research, 57 (2): 1-4, 2017.
doi: 10.1515/jppr-2017-0019
[3] Tran NT, Tran TTH, Do ND, Mai VC. The accumulation of SA- and JA-signaling pathways in the response of Glycine max cv. “Nam Dan” to infestation by Aphis craccivora. Journal of Plant Protection Research, 57 (4): 327-330, 2018.
doi: 10.1515/JPPR-2017-0043
[4] Ortiz J, Marín-Arroyo MR, Noriega-Domínguez MJ, Navarro M, Arozarena, I. Color, phenolics, and antioxidant activity of blackberry (Rubus glaucus Benth.), blueberry (Vaccinium floribundum Kunth.), and apple wines from Ecuador. Journal of Food Science, 78 (7): C985-C993, 2013.
doi: 10.1111/1750-3841.12148
[5] Carrillo-Perdomo E, Aller A, Cruz-Quintana SM, Giampieri F, Álvarez-Suarez JM, Riera ME, Riobamba R. Andean berries from Ecuador: A review on Botany, Agronomy, Chemistry and Health Potential. Journal of Berry Research, 5: 49-69, 2015.
doi: 10.3233/JBR-140093
[6] Horvitz S, Chanaguano D, Arozarena, I. Andean blackberries (Rubus glaucus Benth) quality as affected by harvest maturity and storage conditions. Scientia Horticulturae, 226: 293-301, 2017.
doi: 10.1016/j.scienta.2017.09.002
[7] Mertz C, Cheynier V, Günata Z, Brat P. Analysis of phenolic compounds in two blackberry species (Rubus glaucus and Rubus adenotrichus) by high-performance liquid chromatography with diode array detection and electrospray ion trap mass spectrometry. Journal of Agricultural and Food Chemistry, 55 (21): 8616-8624, 2007.
doi: 10.1021/jf071475d
[8] Lee J, Dossett M, Finn CE. Rubus fruit phenolic research: The good, the bad, and the confusing. Food Chemistry, 130 (4): 785- 796, 2012.
doi: 10.1016/j.foodchem.2011.08.022
[9] Osorio C, Hurtado N, Dawid C, Hofmann T, Heredia-Mira FJ, Morales AL. Chemical characterization of anthocyanins in tamarillo (Solanum betaceum Cav.) and Andes berry (Rubus glaucus Benth.) fruits. Food Chemistry, 132 (4): 1915-1921, 2012.
doi: 10.1016/j.foodchem.2011.12.026
[10] Agronet, “Estadísticas”, 2017.
Retrieved from: https://www.agronet.gov.co/estadistica/Paginas/home.aspx,%202017
[11] Cerón IX, Higuita JC, Cardona CA. Design and analysis of antioxidant compounds from Andes Berry fruits (Rubus glaucus Benth) using an enhanced-fluidity liquid extraction process with CO2 and ethanol. The Journal of Supercritical Fluids, 62: 96-101, 2012.
doi: 10.1016/j.supflu.2011.12.007
[12] Hincapié-Echeverri OD, Saldarriaga-Cardona A, Díaz-Díez C. Biological, botanical and chemical alternatives for the control of blackberry (Rubus glaucus Benth) diseases. Revista Facultad Nacional de Agronomía, 70 (2): 8169-8176, 2017.
doi: 10.15446/rfna.v70n2.64521
[13] Rodríguez-Díaz KJ, Silva-Rojas HV, Boyzo-Marin J, SeguraLedesma SD, Leyva-Mir SG, Rebollar-Alviter Á. Molecular detection of Peronospora sparsa in sources of primary inoculum and components of resistance in wild blackberry species. European Journal of Plant Pathology, 149 (4): 845-851, 2017.
doi: 10.1007/s10658-017-1232-7
[14] Cardona-Hurtado N, Guerrero-Álvarez GE, López-Gutiérrez AM. Identificación de Peronospora sparsa y evaluación del contenido de fenoles en frutos de mora de castilla afectados por este microrganismo. Revista Ceres, 66 (1): 11-17, 2019.
doi: 10.1590/0034-737x201966010002
[15] Fierro-Corrales D, Apodaca-Sánchez MA, QuinteroBenítez JA, Leyva-Mir SG, Flores-Sánchez JL, Tovar-Pedraza JM. Morphological characterization and histopathology of Peronospora ciceris in chickpea (Cicer arietinum L.) leaves and seeds. Revista Chapingo Serie Horticultura, XXI (1): 81-92, 2015.
doi: 10.5154/r.rchsh.2014.02.010
[16] ICONTEC, “NTC 4106. Frutas Frescas. Mora de Castilla. Especificaciones,” Bogotá, 1997. Cardona-Hurtado et al. 2020 313
[17] Guzmán-Nieves CA. Proceso de obtención de un extracto de compuestos fenólicos a partir de orujo de uva tinta Vitis vinifera a bajas temperaturas para aplicación en alimentos y bebidas destinados a consumo humano y animal, México, WO2011062468A2, clasificación A23L33/105, 24 de junio 2011.
https://patents.google.com/patent/WO2011062468A2/es
[18] Velićanski AS, Cvetković DD, Markov SL. Screening of antibacterial activity of raspberry (Rubus idaeus L.) fruit and pomace extracts. Acta Periodica Technologica, 43 (43): 305-313, 2012.
doi: 10.2298/APT1243305V
[19] Abu-Bakar MF, Ismail NA, Isha A, Mei-Ling AL. Phytochemical composition and biological activities of selected wild berries (Rubus moluccanus L., R. fraxinifolius Poir, and R. alpestris Blume). Evidence-Based Complementary and Alternative Medicine, 2016: 110, 2016.
doi: 10.1155/2016/2482930
[20] Guerrero G, Suarez M, Moreno G. Derivados hidroxicinámicos para la discriminación de genotipos de café. Cenicafé, 54 (3): 234- 241, 2004.
[21] Calderón-Oliver M, Escalona-Buendía HB, Medina-Campos ON, Pedraza-Chaverri J, Pedroza-Islas R, Ponce Alquicira E. Optimization of the antioxidant and antimicrobial response of the combined effect of nisin and avocado byproducts. LWT -Food Science and Technology, 65: 46-52, 2016.
doi: 10.1016/j.lwt.2015.07.048
[22] Estupiñan DC, Schwartz SJ, Garzón GA. Antioxidant activity, total phenolics content, anthocyanin, and color stability of isotonic model beverages colored with Andes Berry (Rubus glaucus Benth) anthocyanin powder. Journal of Food Science, 76 (1): S26-S34, 2011.
doi: 10.1111/j.1750-3841.2010.01935.x
[23] Fontaine BM, Nelson K, Lyles JT, Jariwala PB, GarcíaRodriguez JM, Quave CL, Weinert EE. Identification of ellagic acid rhamnoside as a bioactive component of a complex botanical extract with anti-biofilm activity. Frontiers in Microbiology, 8(MAR): 496, 2017.
doi: 10.3389/fmicb.2017.00496
[24] Balasundram N, Sundram K, Samman S. Phenolic compounds in plants and agro-industrial by-products: Antioxidant activity, occurrence, and potential uses. Food Chemistry, 99 (1): 191-203, 2006.
doi: 10.1016/j.foodchem.2005.07.042
[25] Sharma OP, Bhat TK. DPPH antioxidant assay revisited. Food Chemistry, 113 (4): 1202-1205, 2009.
doi: 10.1016/j.foodchem.2008.08.008
[26] Prior RL, Wu X, Schaich K. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. Journal of Agricultural and Food Chemistry, 53 (10): 4290-4302, 2005.
doi: 10.1021/jf0502698
[27] Jones A, Pravadali-Cekic S, Dennis GR, Bashir R, Mahon PJ, Shalliker RA. Ferric reducing antioxidant potential (FRAP) of antioxidants using reaction flow chromatography. Analytica Chimica Acta, 967: 93-101, 2017.
doi: 10.1016/J.ACA.2017.02.032
[28] Vasco C, Ruales J, Kamal-Eldin A. Total phenolic compounds and antioxidant capacities of major fruits from Ecuador. Food Chemistry, 111 (4): 816-823, 2008.
doi: 10.1016/j.foodchem.2008.04.054
[29] Bernal LJ, Melo LA, Díaz Moreno C. Evaluation of the antioxidant properties and aromatic profile during maturation of the blackberry (Rubus glaucus Benth) and the bilberry (Vaccinium meridionale Swartz). Revista Facultad Nacional de Agronomía, 67 (1): 7209-7218, 2014.
doi: 10.15446/rfnam. v67n1.42649
[30] Wang SY, Lin HS. Antioxidant activity in fruits and leaves of blackberry, raspberry, and strawberry varies with cultivar and developmental stage. Journal of Agricultural and Food Chemistry, 48 (2): 140-146, 2000.
doi: 10.1021 / jf9908345
[31] Sellappan S, Akoh CC, Krewer G. Phenolic compounds and antioxidant capacity of Georgia-grown blueberries and blackberries. Journal of Agricultural and Food Chemistry, 50 (8): 2432-2438, 2002.
doi: 10.1021/jf011097r
[32] Garzón G, Riedl K., Schwartz S. Determination of anthocyanins, total phenolic content, and antioxidant activity in Andes berry (Rubus glaucus Benth). Food Science, 74 (3): C227-C232, 2009.
doi: 10.1111/j.1750-3841.2009.01092.x
[33] Zacarés L, López-Gresa MP, Fayos J, Primo J, Bellés JM, Conejero V. Induction of p-coumaroyldopamine and feruloyldopamine, two novel metabolites, in tomato by the bacterial pathogen Pseudomonas syringae. Molecular Plant-Microbe Interactions, 20 (11): 1439-1448, 2007.
doi: 10.1094/MPMI-20-11-1439
[34] Ribera A, Zuñiga G. Induced plant secondary metabolites for phytopathogenic fungi control: A review. Journal of Soil Science and Plant Nutrition, 12 (4): 893-911, 2012.
doi: 10.4067/S0718-95162012005000040
[35] Mikulic-Petkovsek M, Schmitzer V, Stampar F, Veberic R, Koron D. Changes in phenolic content induced by infection with Didymella applanata and Leptosphaeria coniothyrium, the causal agents of raspberry spur and cane blight. Plant Pathology, 63(1): 185-192, 2014.
doi: 10.1111/ppa.12081
[36] Badhani B, Sharma N, Kakkar R. Gallic acid: a versatile antioxidant with promising therapeutic and industrial applications. RSC Advances, 5 (35): 27540-27557, 2015.
doi: 10.1039/C5RA01911G
[37] Do QD, Angkawijaya AE, Tran-Nguyen PL, Huynh LH, Soetaredjo FE, Ismadji S, Ju YH. Effect of extraction solvent on total phenol content, total flavonoid content, and antioxidant activity of Limnophila aromatica. Journal of Food and Drug Analysis, 22 (3): 296-302, 2014.
doi: 10.1016/J.JFDA.2013.11.001
[38] Carbonel KN, Suárez-Cunza S, Arnao I. Características fisicoquímicas y capacidad antioxidante in vitro del extracto de Gentianella nitida. Anales de la Facultad de Medicina, 77 (4): 333-337, 2016.
doi: 10.15381/anales. v77i4.12648
[39] Paredes-López O, Cervantes-Ceja ML, Vigna-Pérez M, Hernández-Pérez T. Berries: Improving human health and healthy aging and promoting quality life—A Review. Plant Foods for Human Nutrition, 65 (3): 299-308, 2010.
doi: 10.1007/s11130-010-0177-1
How to Cite
Cardona-Hurtado, N., Guerrero-Alvarez, G. E., & López-Gutiérrez, A. M. (2020). Changes in phenolic compounds and antioxidant capacity of Andean raspberries in response to Peronospora sparsa. Universitas Scientiarum, 25(2), 299–319. https://doi.org/10.11144/Javeriana.SC25-2.cipc
Issue
Section
Food Chemistry