Evaluation of antioxidant activity, polyphenolic compounds, amino acids and mineral elements of representative genotypes of Lonicera edulis

Sochor, Jiří; Juríková, Tünde; Pohanka, Miroslav; Škutková, Helena; Baroň, Mojmír; Tomášková, Lenka; Balla, Štefan; Klejdus, Bořivoj; Pokluda, Robert; Mlček, Jiří; Trojáková, Zuzana; Šaloun, Jan

dc.title	Evaluation of antioxidant activity, polyphenolic compounds, amino acids and mineral elements of representative genotypes of Lonicera edulis	en
dc.contributor.author	Sochor, Jiří
dc.contributor.author	Juríková, Tünde
dc.contributor.author	Pohanka, Miroslav
dc.contributor.author	Škutková, Helena
dc.contributor.author	Baroň, Mojmír
dc.contributor.author	Tomášková, Lenka
dc.contributor.author	Balla, Štefan
dc.contributor.author	Klejdus, Bořivoj
dc.contributor.author	Pokluda, Robert
dc.contributor.author	Mlček, Jiří
dc.contributor.author	Trojáková, Zuzana
dc.contributor.author	Šaloun, Jan
dc.relation.ispartof	Molecules
dc.identifier.issn	1420-3049 Scopus Sources, Sherpa/RoMEO, JCR
dc.date.issued	2014
utb.relation.volume	19
utb.relation.issue	5
dc.citation.spage	6504
dc.citation.epage	6523
dc.type	article
dc.language.iso	en
dc.publisher	MDPI AG
dc.identifier.doi	10.3390/molecules19056504
dc.relation.uri	http://www.mdpi.com/1420-3049/19/5/6504
dc.relation.uri	https://www.mdpi.com/1420-3049/19/5/6504/pdf?version=1403117887
dc.subject	Amino acids	en
dc.subject	Antioxidant activity	en
dc.subject	Bioinformatics analysis	en
dc.subject	Lonicera edulis	en
dc.subject	Mineral compounds	en
dc.subject	Phenolic compounds	en
dc.description.abstract	The aim of this study was to evaluate the bioactive substances in 19 berry cultivars of edible honeysuckle (Lonicera edulis). A statistical evaluation was used to determine the relationship between the content of selected bioactive substances and individual cultivars. Regarding mineral elements, the content of sodium was measured using potentiometry and spectrophotometry. The content of selected polyphenolic compounds with high antioxidant activity was determined by a HPLC-UV/ED method. The total amount of polyphenols was determined by the Folin-Ciocalteu method. The antioxidant activity was determined using five methods (DPPH, FRAP, ABTS, FR and DMPD) that differ in their principles. The content of 13 amino acids was determined by ion-exchange chromatography. The experimental results obtained for the different cultivars were evaluated and compared by statistical and bioinformatic methods. A unique feature of this study lies in the exhaustive analysis of the chosen parameters (amino acids, mineral elements, polyphenolic compounds and antioxidant activity) during one growing season. © 2014 by the authors.	en
utb.faculty	Faculty of Technology
dc.identifier.uri	http://hdl.handle.net/10563/1003775
utb.identifier.obdid	43871825
utb.identifier.scopus	2-s2.0-84901472544
utb.identifier.wok	000337113000066
utb.identifier.coden	MOLEF
utb.source	j-scopus
dc.date.accessioned	2014-07-07T13:43:54Z
dc.date.available	2014-07-07T13:43:54Z
dc.rights	Attribution-NonCommercial-NoDerivs 3.0 Unported
dc.rights.uri	https://creativecommons.org/licenses/by-nc-nd/3.0/
dc.rights.access	openAccess
utb.contributor.internalauthor	Mlček, Jiří
utb.fulltext.affiliation	Jiri Sochor 1,2,, Tunde Jurikova 3, Miroslav Pohanka 4,5, Helena Skutkova 6, Mojmir Baron 1, Lenka Tomaskova 1, Stefan Balla 3, Borivoj Klejdus 2, Robert Pokluda 7, Jiri Mlcek 8, Zuzana Trojakova 9 and Jan Saloun 10 1 Department of Viticulture and Enology, Faculty of Horticulture, Mendel University, Valticka 337, CZ-691 44 Lednice, Czech Republic; E-Mails: mojmirbaron@seznam.cz (M.B.); tomaskova.l.9@gmail.com (L.T.) 2 Department of Chemistry and Biochemistry, Faculty of Agronomy, Mendel University, Zemedelska 1, CZ-613 00 Brno, Czech Republic; E-Mail: borivoj.klejdus@mendelu.cz 3 Institute for Teacher Training, Faculty of Central European Studies, Constantine the Philosopher University, Drazovska 4, SK-949 74 Nitra, Slovak Republic; E-Mails: tjurikova@ukf.sk; (T.J.); sballa@ukf.sk (S.B.) 4 Faculty of Military Health Sciences, University of Defence, Trebesska 1575, CZ-500 01 Hradec Kralove, Czech Republic; E-Mail: miroslav.pohanka@gmail.com 5 Karel English College, Sujanovo namesti 356/1, 60200 Brno, Czech Republic 6 Department of Biomedical Engineering, Faculty of Electrical Engineering and Communication, Brno University of Technology, Kolejni 4, CZ-612 00 Brno, Czech Republic; E-Mail: skutkova@feec.vutbr.cz 7 Department of Vegetable Science and Floriculture, Faculty of Horticulture, Mendel University, Lednice, Valtická 337, CZ-691 44 Lednice, Czech Republic; E-Mail: pokluda@mendelu.cz 8 Department of Food Analysis and Chemistry, Faculty of Technology, Tomas Bata University, Namesti T.G.Masaryka 275, 762 72 Zlin, Czech Republic; E-Mail: mLcek@ft.utb.cz 9 Department of Garden and Landscape Architecture, Faculty of Horticulture, Mendel University, Valticka 337, CZ-691 44 Lednice, Czech Republic; E-Mail: xtrojak2@node.mendelu.cz 10 Department of Applied Pharmacy, Faculty of Pharmacy, University of Veterinary and Pharmaceutical Sciences, Palackeho 1, CZ-612 42 Brno, Czech Republic; E-Mail: jan_saloun@post.cz Author to whom correspondence should be addressed; E-Mail: sochor.jirik@seznam.cz; Tel.: +420-519-367-211; Fax: +420-519-367-222.
utb.fulltext.dates	Received: 26 January 2014 Received in revised form: 16 May 2014 Accepted: 16 May 2014 Published: 21 May 2014
utb.fulltext.references	1. Plekhanova, M.N.; Streltsyna, S.A.; Rostova, N.S. Fruit Chemical Composition of Lonicera subsect Caerulea (Caprifoliaceae species), Genetic Resourses in Russia and Neighbouring Countries; Estonian Agricultural University-Forest Research Institut: Tartu, Estonia, 1998; Volume 30, pp. 143–146. 2. Pokorna-Jurikova, T.; Matuskovic, J. The study of irrigation influence on nutritional value of Lonicera kamtschatica—Cultivar Gerda 25 and Lonicera edulis berries under the Nitra conditions during 2001–2003. Hortic. Sci. 2007, 34, 11–16. 3. Jurikova, T.; Rop, O.; Mlcek, J.; Sochor, J.; Balla, S.; Szekeres, L.; Hegedusova, A.; Hubalek, J.; Adam, V.; Kizek, R. Phenolic profile of edible honeysuckle berries (Genus lonicera) and their biological effects. Molecules 2012, 17, 61–79. 4. Jurikova, T.; Sochor, J.; Rop, O.; Mlcek, J.; Balla, S.; Szekeres, L.; Zitny, R.; Zitka, O.; Adam, V.; Kizek, R. Evaluation of polyphenolic profile and nutritional value of non-traditional fruit species in the Czech Republic—A comparative study. Molecules 2012, 17, 8968–8981. 5. Gazdik, Z.; Krska, B.; Adam, V.; Saloun, J.; Pokorna, T.; Reznicek, V.; Horna, A.; Kizek, R. Electrochemical determination of the antioxidant potential of some less common fruit species. Sensors 2008, 8, 7564–7570. 6. Lefèvre, I.; Ziebel, J.; Guignard, C.; Sorokin, A.; Tikhonova, O.; Dolganova, N.; Hoffmann, L.; Eyzaguirre, P.; Hausman, J.-F. Evaluation and comparison of nutritional quality and bioactive compounds of berry fruits from Lonicera caerulea, Ribes L. species and Rubus idaeus grown in Russia. J. Berry Res. 2011, 1, 159–167. 7. Rop, O.; Reznicek, V.; Mlcek, J.; Jurikova, T.; Balik, J.; Sochor, J.; Kramarova, D. Antioxidant and radical oxygen species scavenging activities of 12 cultivars of blue honeysuckle fruit. Hortic. Sci. 2011, 38, 63–70. 8. Myjavcova, R.; Marhol, P.; Kren, V.; Simanek, V.; Ulrichova, J.; Palikova, I.; Papouskova, B.; Lemr, K.; Bednar, P. Analysis of anthocyanin pigments in Lonicera (Caerulea) extracts using chromatographic fractionation followed by microcolumn liquid chromatography-mass spectrometry. J. Chromatogr. A 2010, 1217, 7932–7941. 9. Chaovanalikit, A.; Thompson, M.M.; Wrolstad, R.E. Characterization and quantification of Anthocyanins and polyphenolics in blue honeysuckle (Lonicera caerulea L.). J. Agric. Food Chem. 2004, 52, 848–852. 10. Palikova, I.; Heinrich, J.; Bednar, P.; Marhol, P.; Kren, V.; Cvak, L.; Valentova, K.; Ruzicka, F.; Hola, V.; Kolar, M.; et al. Constituents and Antimicrobial Properties of Blue Honeysuckle: A Novel Source for Phenolic Antioxidants. J. Agric. Food Chem. 2008, 56, 11883–11889. 11. Farcasanu, I.C.; Gruia, M.I.; Paraschivescu, C.; Oprea, E.; Baciu, I. Ethanol extracts of Lonicera caerulea and Sambucus nigra berries exhibit antifungal properties upon heat-stressed Saccharomyces cerevisiae cells. Rev. Chim. 2006, 57, 79–81. 12. Gruia, M.I.; Oprea, E.; Gruia, I.; Negoita, V.; Farcasanu, I.C. The Antioxidant Response Induced by Lonicera caerulaea Berry Extracts in Animals Bearing Experimental Solid Tumors. Molecules 2009, 14, 893–893. 13. Thompson, M.M.; Chaovanalikit, A. Preliminary Observations on Adaptation and Nutraceutical Values of Blue Honeysuckle (Lonicera caerulea) in Oregon, USA. In Berry Crop Breeding, Production and Utilization for a New Century; Hicklenton, P., Maas, J., Eds.; 26th International Horticultural Congress: Toronto, ON, Canada, 2003; pp. 65–72. 14. Zhao, H.T.; Wang, Z.Y.; Cheng, C.L.; Yao, L.; Wang, L.; Lu, W.H.; Yang, X.; Ma, F.M. In-vitro free radical scavenging activities of anthocyanins from three berries. J. Med. Plants Res. 2011, 5, 7036–7042. 15. Kusznierewicz, B.; Piekarska, A.; Mrugalska, B.; Konieczka, P.; Namiesnik, J.; Bartoszek, A. Phenolic composition and antioxidant properties of polish blue-berried honeysuckle genotypes by HPLC-DAD-MS, HPLC postcolumn derivatization with ABTS or FC, and TLC with DPPH visualization. J. Agric. Food Chem. 2012, 60, 1755–1763. 16. Švarcova, I.; Heinrich, J.; Valentova, K. Berry fruits as a source of biologically active compounds: The case of Lonicera caerulea. Biomed. Pap. Med. Fac. Univ. Palacky Olomouc 2007, 151, 163–174. 17. Skupien, K.; Ochmian, I.; Grajkowski, J. Influence of ripening time on fruit chemical composition of two blue honeysuckle cultigens. J. Fruit Ornam. Plant Res. 2009, 17, 101–111. 18. Ochmian, I.; Skupien, K.; Grajkowski, J.; Smolik, M.; Ostrowska, K. Chemical Composition and Physical Characteristics of Fruits of Two Cultivars of Blue Honeysuckle (Lonicera caerulea L.) in Relation to their Degree of Maturity and Harvest Date. Not. Bot. Horti Agrobot. Cluj-Napoca 2012, 40, 155–162. 19. Rupasinghe, H.P.V.; Yu, L.J.; Bhullar, K.S.; Bors, B. Short communication: Haskap (Lonicera caerulea): A new berry crop with high antioxidant capacity. Can. J. Plant Sci. 2012, 92, 1311–1317. 20. Streltsyna, S.A.; Sorotkin, A.A.; Plekhanova, M.N.; Lobanova, E.V. Sostav biologičeskich aktivnyh fenolyj soedinenii sortov žimolosti v uslovjach everno-zapadnoj zony plodovodstva. Agrar. Ross. 2006, 6, 67–72 21. Bakowska-Barczak, A.M.; Marianchuk, M.; Kolodziejczyk, P. Survey of bioactive components in Western Canadian berries. Can. J. Physiol. Pharmacol. 2007, 85, 1139–1152. 22. Vasco, C.; Ruales, J.; Kamal-Eldin, A. Total phenolic compounds and antioxidant capacities of major fruits from Ecuador. Food Chem. 2008, 111, 816–823. 23. Plekhanova, M.N. Blue Honeysuckle (Lonicera caerulea L.)—A New Commercial Berry Crop for Temperate Climate: Genetic Resources and Breeding. In Proceedings of the Eucarpia Symposium on Fruit Breeding and Genetics, Dresden, Germany, 6–10 September 1999; Geibel, M., Fischer, M., Fischer, C., Eds.; International Society Horticultural Science: Leuven, Belgium, 2000; Volumes 1 and 2, pp. 159–164. 24. Zadernowski, R.; Naczk, M.; Nesterowicz, J. Phenolic acid profiles in some small berries. J. Agric. Food Chem. 2005, 53, 2118–2124. 25. Orincak, J.; Matuskovic, J.; Jurcak, S. Possibilities of Species Lonicera caerulea in Utilization of the Secondary Metabolism in Food and Pharmaceutical Processing, 1st ed.; SPU: Nitra, Slovakia, 2003; pp. 210–219. 26. Deineka, V.I.; Sorokopudov, V.N.; Deineka, L.A.; Shaposhnik, E.I.; Koltsov, S.V. Anthocyans from fruit of some plants of the Caprifoliaceae family. Chem. Nat. Compd. 2005, 41, 162–164. 27. Manach, C.; Scalbert, A.; Morand, C.; Remesy, C.; Jimenez, L. Polyphenols: Food sources and bioavailability. Am. J. Clin. Nutr. 2004, 79, 727–747. 28. Oszmianski, J.; Wojdylo, A. Aronia melanocarpa phenolics and their antioxidant activity. Eur. Food Res. Technol. 2005, 221, 809–813. 29. Li, H.Y.; Deng, Z.Y.; Wu, T.; Liu, R.H.; Loewen, S.; Tsao, R. Microwave-assisted extraction of phenolics with maximal antioxidant activities in tomatoes. Food Chem. 2012, 130, 928–936. 30. Jurikova, T.; Matuskovic, J.; Gazdik, Z. Effect of irrigation on intensity of respiration and study of sugar and organic acids content in different development stages of Lonicera kamtschatica and Lonicera edulis berries. Hortic. Sci. 2009, 36, 14–20. 31. Gazdik, Z.; Reznicek, V.; Adam, V.; Zitka, O.; Jurikova, T.; Krska, B.; Matuskovic, J.; Plsek, J.; Saloun, J.; Horna, A.; et al. Use of Liquid Chromatography with Electrochemical Detection for the Determination of Antioxidants in Less Common Fruits. Molecules 2008, 13, 2823–2836. 32. Ochmian, I.; Grajkowski, J.; Skupien, K. Field performance, fruit chemical composition and formness under cold storage and stimulated “shelf–life” conditions of tree blue honeysuckle cultigens (Lonicera caerulea). J. Fruit Ornam. Plant Res. 2008, 16, 83–91. 33. Hakkinen, S.H.; Karenlampi, S.O.; Heinonen, I.M.; Mykkanen, H.M.; Torronen, A.R. HPLC method for screening of flavonoids and phenolic acids in berries. J. Sci. Food Agric. 1998, 77, 543–551. 34. Jurikova, T.; Sochor, J.; Rop, O.; Mlcek, J.; Balla, S.; Szekeres, L.; Adam, V.; Kizek, R. Polyphenolic profile and biological activity of Chinese hawthorn (Crataegus pinnatifida BUNGE) fruits. Molecules 2012, 17, 14490–14509. 35. Smolik, M.; Ochmian, I.; Grajkowski, J. Genetic variability of Polish and Russian accessions of cultivated blue honeysuckle (Lonicera caerulea). Russ. J. Genet. 2010, 46, 960–966. 36. Benzie, I.F.F.; Strain, J.J. Ferric reducing antioxidant power assay: Direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol. 1999, 299, 15–27. 37. Wang, H.; Cao, G.H.; Prior, R.L. Total antioxidant capacity of fruits. J. Agric. Food Chem. 1996, 44, 701–705. 38. Rop, O.; Posolda, M.; Mlcek, J.; Reznicek, V.; Sochor, J.; Adam, V.; Kizek, R.; Sumczynski, D. Qualities of native apple cultivar juices characteristic of Central Europe. Not. Bot. Horti Agrobot. Cluj-Napoca 2012, 40, 222–228. 39. Rop, O.; Sochor, J.; Jurikova, T.; Zitka, O.; Skutkova, H.; Mlcek, J.; Salas, P.; Krska, B.; Babula, P.; Adam, V.; et al. Effect of five different stages of ripening on chemical compounds in medlar (Mespilus germanica L.). Molecules 2011, 16, 74–91. 40. Sochor, J.; Skutkova, H.; Babula, P.; Zitka, O.; Cernei, N.; Rop, O.; Krska, B.; Adam, V.; Provaznik, I.; Kizek, R. Mathematical Evaluation of the Amino Acid and Polyphenol Content and Antioxidant Activities of Fruits from Different Apricot Cultivars. Molecules 2011, 16, 7428–7457. 41. Rop, O.; Balik, J.; Reznicek, V.; Jurikova, T.; Skardova, P.; Salas, P.; Sochor, J.; Mlcek, J.; Kramarova, D. Chemical characteristics of fruits of some selected quince (Cydonia oblonga Mill.) cultivars. Czech J. Food Sci. 2011, 29, 65–73. 42. Rop, O.; Jurikova, T.; Sochor, J.; Mlcek, J.; Kramarova, D. Antioxidant capacity, scavenging radical activity and selected chemical composition of native apple cultivars from central Europe. J. Food Qual. 2011, 34, 187–194. 43. Koracevic, D.; Koracevic, G.; Djordjevic, V.; Andrejevic, S.; Cosic, V. Method for the measurement of antioxidant activity in human fluids. J. Clin. Pathol. 2001, 54, 356–361. 44. Sochor, J.; Babula, P.; Krska, B.; Horna, A.; Provaznik, I.; Hubalek, J.; Kizek, R. Evaluation of output signals from CoulArray detector for determination of antioxidant capacity of apricots samples. In Analysis of Biomedical Signals and Images; Jan, J., Jirik, R., Kolar, R., Kolarova, J., Kozumplik, J., Provaznik, I., Eds.; Brno Univ Technology Vut Press: Brno, Czech Republic, 2010; pp. 209–214. 45. Prior, R.L.; Wu, X.L.; Schaich, K. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J. Agric. Food Chem. 2005, 53, 4290–4302. 46. Pohanka, M.; Stetina, R.; Svobodova, H.; Ruttkay-Nedecky, B.; Jilkova, M.; Sochor, J.; Sobotka, J.; Adam, V.; Kizek, R. Sulfur mustard causes oxidative stress and depletion of antioxidants in muscles, livers, and kidneys of Wistar rats. Drug Chem. Toxicol. 2013, 36, 270–276. 47. Pohanka, M.; Sochor, J.; Ruttkay-Nedecky, B.; Cernei, N.; Adam, V.; Hubalek, J.; Stiborova, M.; Eckschlager, T.; Kizek, R. Automated assay of the potency of natural antioxidants using pipetting robot and spectrophotometry. J. Appl. Biomed. 2012, 10, 155–167. 48. Raudsepp, P.; Anton, D.; Roasto, M.; Meremae, K.; Pedastsaar, P.; Maesaar, M.; Raal, A.; Laikoja, K.; Pussa, T. The antioxidative and antimicrobial properties of the blue honeysuckle (Lonicera caerulea L.), Siberian rhubarb (Rheum rhaponticum L.) and some other plants, compared to ascorbic acid and sodium nitrite. Food Control 2013, 31, 129–135. 49. Paulovicsova, B.; Turianica, I.; Jurikova, T.; Baloghova, M.; Matuskovic, J. Antioxidant properties of selected less common fruit species. Lucrări ştiinţifice Zootehnie şi Biotehnologii 2009, 42, 608–614. 50. Lee, J.; Schreiner, R.P. Free amino acid profiles from “Pinot noir” grapes are influenced by vine N-status and sample preparation method. Food Chem. 2010, 119, 484–489. 51. Wallrauch, S. Amino-acids criteria for the evaluation of fruit juices. Abstr. Pap. Am. Chem. Soc. 1985, 189, 0065–7727. 52. Zitka, O.; Sochor, J.; Rop, O.; Skalickova, S.; Sobrova, P.; Zehnnalek, J.; Beklova, M.; Krska, B.; Adam, V.; Kizek, R. Comparison of various easy-to-use procedures for extraction of phenols from apricot fruits. Molecules 2011, 16, 2914–2936. 53. Singleton, V.L.; Orthofer, R.; Lamuela-Raventos, R.M. Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. In Oxidants and Antioxidants, Part A; Packer, L., Ed.; Gulf Professional Publishing: San Diego, CA, USA, 1999; pp. 152–178. 54. Sochor, J.; Ryvolova, M.; Krystofova, O.; Salas, P.; Hubalek, J.; Adam, V.; Trnkova, L.; Havel, L.; Beklova, M.; Zehnalek, J.; et al. Fully automated spectrometric protocols for determination of antioxidant activity: Advantages and disadvantages. Molecules 2010, 15, 8618–8640. 55. Sochor, J.; Salas, P.; Zehnalek, J.; Krska, B.; Adam, V.; Havel, L.; Kizek, R. An assay for spectrometric determination of antioxidant activity of a biological extract. Listy Cukrov. 2010, 126, 416–417.
utb.fulltext.sponsorship	The work was supported by OP Education for Competitiveness (European Social Fund and the state budget of the Czech Republic) CZ.1.07/2.4.00/17.0045 Support of international cooperation - multidisciplinary themes in life and material sciences. This work was realised in CEITEC - Central European Institute of Technology with research infrastructure supported by the project CZ.1.05/1.1.00/02.0068 financed from European Regional Development Fund. Author Jiri Sochor would like to express his thanks for CZ.1.07/2.3.00/30.0017 Postdocs in Biological Sciences at MENDELU support.
utb.fulltext.projects	CZ.1.07/2.4.00/17.0045
utb.fulltext.projects	CZ.1.05/1.1.00/02.0068
utb.fulltext.projects	CZ.1.07/2.3.00/30.0017
utb.fulltext.faculty	Faculty of Applied Informatics
utb.fulltext.ou	Department of Mathematics