Stimulation of plant secondary metabolites synthesis in soilless cultivated strawberries (Fragaria × ananassa Duchesne) using zinc-alginate microparticles

Stimulation of plant secondary metabolites synthesis in soilless cultivated strawberries (Fragaria × ananassa Duchesne) using zinc-alginate microparticles

An innovative approach to stimulate the production of plant secondary metabolites (PSM) is the use of encapsulated bioactive agents. Zinc-alginate microparticles [microspheres (ALG/Zn) and microcapsules (CS/ALG/Zn)] were applied near the root zone of soilless cultivated strawberries (Fragaria × ananassa Duchesne) to ensure a constant supply of an essential micronutrient zinc ions throughout the whole period of maturation. Both, ALG/Zn and CS/ALG/Zn had a positive effect on PSM (total polyphenols, total flavonoids, total anthocyanins, and flavan-3-ols) synthesis and increased antioxidant activity in two strawberry varieties (Albion and San Andreas). Treatments with Zn-alginate microparticles resulted in no visible damages on the plant and fruits. A two-year study revealed an increase of ~34% in total polyphenolic compounds and ~23% in total flavonoids in the San Andreas variety. The highest increase in antioxidant activity [ABTS (~37%) and DPPH (~38%)] was observed in the San Andreas variety treated with CS/ALG/Zn. Respectively high increase in anthocyanins was observed in both varieties (~54% and ~61%, respectively) treated with CS/ALG/Zn. Treatments with zinc-alginate microparticles resulted in a successful stimulation of PSM synthesis and increased strawberries’ nutritive value. Encapsulation of zinc ions proved to be simple, sustainable, and environmentally favorable to produce strawberries fortified with important bioactive compounds.

___

  • Adorno WT, RezzadoriK, Arend GD, Chaves VC, ReginattoFH et al. (2016). Enhancement of phenolic compounds content and antioxidant activity of strawberry (Fragaria × ananassa) juice by block freeze concentration technology. International Journal of Food Science & Technology 52 (3): 781-787. doi: 10.1111/ijfs.13335
  • Brand-Williams W, Cuvelier ME, Berset C (1995). Use of a free radical method to evaluate antioxidant activity. LWT - Food Science and Technology 28 (1): 25-30. doi: 10.1016/S0023- 6438(95)80008-5
  • Cakmak I, Marschner H (1993). Effect of zinc nutritional status on activities of superoxide radical and hydrogen peroxide scavenging enzymes in bean leaves. In: Barrow NJ (editor). Plant Nutrition — from Genetic Engineering to Field Practice. Developments in Plant and Soil Sciences, Vol. 54. Dordrecht, Netherlands: Springer. doi: 10.1007/978-94-011-1880-4_21
  • Cakmak I (2000). Role of zinc in protecting plant cells from reactive oxygen species. New Phytologist 146 (1): 185-205. doi: 10.1046/j.1469-8137.2000.00630.x
  • Derakhshani Z, Hassani A, Sadaghiani MHR, Hassanpouraghdam MB, Khalifani BH et al. (2011). Effect of zinc application on growth and some biochemical characteristics of costmary (Chrysanthemum balsamita L.). Communications in Soil Science and Plant Analysis 42 (20): 2493-2503. doi: 10.1080/00103624.2011.609257
  • Di Vittori L, Mazzoni L, Battino M, Mezzetti B (2018). Pre-harvest factors influencing the quality of berries. Scientia Horticulturae 233 (1): 310-322. doi: 10.1016/j.scienta.2018.01.058
  • Díaz-García MC, Obón JM, Castellar MR, Collado J, Alacid M (2013). Quantification by UHPLC of total individual polyphenols in fruit juices. Food Chemistry 138 (2-3): 938-949. doi: 10.1016/j. foodchem.2012.11.061
  • Doolette CL, Read TL, Li C, Scheckel KG, Donner E et al. (2018). Foliar application of zinc sulphate and zinc EDTA to wheat leaves: Differences in mobility, distribution, and speciation. Journal of Experimental Botany 69 (18): 4469-4481. doi: 10.1093/jxb/ ery236.
  • Duralija B, Cmelik Z, Druzic Orlic J, Milicevic T (2006). The effect of planting system on the yield of strawberry grown out-ofseason. Acta Horticulturae 708 (1): 89-92. doi: 10.17660/ ActaHortic.2006.708.11
  • El‐Sawi SA, Mohamed MA (2002). Cumin herb as a new source of essential oils and its response to foliar spray with some micro‐ elements. Food Chemistry 77 (1): 75-80. doi: 10.1016/S0308- 8146(01)00326-0
  • Fageria NK, Baligar VC, Clark RB (2002). Micronutrients in crop production. Advances in Agronomy 77 (1): 189-272. doi: 10.1016/ S0065-2113(02)77015-6
  • Farid MZ, Qureshi KM, Shah SH, Qureshi AA, Umair M et al. (2020). Foliar application of micronutrients improves growth, productivity and fruit quality of strawberry. The Journal of Animal & Plant Sciences 30 (4): 905-912. doi: 10.36899/JAPS.2020.4.0106
  • Fuleki T, Francis FJ (1968). Quantitative methods for anthocyanins: 1. extraction and determination of total anthocyanins in cranberries. Journal of Food Science 33 (3): 266-274. doi: 10.1111/j.1365- 2621.1968.tb00887.x
  • Garzon GA, Wrolstad RE (2002). Comparison of the stability of pelargonidin-based anthocyanins in strawberry juice and concentrate. Journal of Food Science 67 (4): 1288-1299. doi: 10.1111/j.1365-2621.2002.tb10277.x
  • Giamperi F, Tulipani S, Alvarez-Suarez JM, Quiles JL, Mezzetti B et al. (2012). The strawberry: composition, nutritional quality, and impact on human health. Nutrition 28 (1): 9-19. doi: 10.1016/j. nut.2011.08.009
  • Giampieri F, Alvarez-Suarez JM, Cordero MD, Gasparrini M, ForbesHernandez TY et al. (2017). Strawberry consumption improves aging-associated impairments, mitochondrial biogenesis and functionality through the AMP-activated protein kinase signaling cascade. Food Chemistry 34 (1): 464-471. doi: 10.1016/j. foodchem.2017.05.017
  • Gill SS, Anjum NA, Gill R, Yadav S, Hasanuzzaman M et al. (2015). Superoxide dismutase-mentor of abiotic stress tolerance in crop plants. Environmental Science and Pollution Research 22 (1): 10375-10394. doi: 10.1007/s11356-015-4532-5
  • Grotz N, Guerinot ML (2006). Molecular aspects of Cu, Fe and Zn homeostasis in plants. Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1763 (7): 595-608. doi: 10.1016/j. bbamcr.2006.05.014
  • Gupta N, Ram H, Kumar B (2016). Mechanism of Zinc absorption in plants: uptake, transport, translocation and accumulation. Reviews in Environmental Science and Biotechnology 15: 89-109. doi: 10.1007/s11157-016-9390-1
  • Ivanova V, Stefova M, Chinnici F(2010). Determination of the polyphenol contents in Macedonian grapes and wines by standardized spectrophotometric methods. Journal of Serbian Chemical Society 75 (1): 45-59.doi: 10.2298/JSC1001045I
  • Jurić S, Đermić E, Topolovec-Pintarić S, Bedek M, Vinceković M (2019a). Physicochemical properties and release characteristics of calcium alginate microspheres loaded with Trichoderma viride spores. Journal of Integrative Agriculture 18 (11): 2534- 2548. doi: 10.1016/S2095-3119(19)62634-1
  • Jurić S, Šegota S, Vinceković M (2019b). Influence of surface morphology and structure of alginate microparticles on the bioactive agents release behavior. Carbohydrate Polymers 218 (1): 234-242. doi: 10.1016/j.carbpol.2019.04.096
  • Jurić S, Sopko Stracenski K, Król-Kilinska Ż, Žutić I et al. (2020). The enhancement of plant secondary metabolites contents in Lactuca sativa L. by encapsulated bioactive agents. Scientific Reports 10 (1): 3737. doi: 10.1038/s41598-020-60690-3
  • Kårlund A, Hanhineva K, Lehtonen M, Karjalainen RO, Sandell M (2015). Nontargeted metabolite profiles and sensory properties of strawberry cultivars grown both organically and conventionally. Journal of Agricultural and Food Chemistry 63 (3): 1010-1019. doi: 10.1021/jf505183j
  • Kazemi M (2014). Influence of foliar application of iron, calcium and zinc sulfate on vegetative growth and reproductive characteristics of strawberry cv. ‘Pajaro’. Trakia Journal of Sciences 12 (1): 21-26.
  • Manzeke GM, Mtambanengwe F, Nezomba H, Mapfumo P (2014). Zinc fertilization influence on maize productivity and grain nutritional quality under integrated soil fertility management in Zimbabwe. Field Crops Research 166 (1): 128-136. doi: 10.1016/j.fcr.2014.05.019
  • Michalska A, Carlen C, Heritier J, Andlauer W (2017). Profiles of bioactive compounds in fruits and leaves of strawberry cultivars. Journal of Berry Research 7 (2): 71-84. doi: 10.3233/ JBR-160146
  • Misra A, Sharma S (1991). Critical Zn concentration for essential oil yield and menthol concentration of Japanese mint. Fertilizer Research 29 (1): 261-265. doi: 10.1007/BF01052394
  • Oszmiański J, Wojdyło A(2008). Comparative study of phenolic content and antioxidant activity of strawberry puree, clear, and cloudy juices. European Food Research and Technology 228 (4): 623-631. doi: 10.1007/s00217-008-0971-2
  • RadićS, Vujčić V, Glogoški M, Radić-Stojković M (2016). Influence of pH and plant growth regulators on secondary metabolite production and antioxidant activity of Stevia rebaudiana (Bert). Periodicum Biologorum 118 (1): 9-19. doi: 10.18054/ pb.2016.118.1.3420
  • Re R, Pellegrini N, Proteggente A, Pannala A, Yang M et al. (1999). Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology and Medicine 26 (9- 10): 1231-1237. doi: 10.1016/S0891-5849(98)00315-3
  • Rezaeieh KAP, Gurbuz B, Eivazi A (2016). Effects of different zinc levels on vegetative growth and essential oil contents of some Iranian and Turkish cumin (Cuminum cyminum L.) genotypes. Journal of Essential Oil Bearing Plants 19 (5): 1181-1191. doi: 10.1080/0972060X.2016.1186573
  • Šamec D, Maretic M, Lugaric I, Mešic A, Salopek-Sondi B et al. (2016).Assessment of the differences in the physical, chemical and phytochemical properties of four strawberry cultivars using principal component analysis. Food Chemistry 194 (1): 828-834. doi: 10.1016/j.foodchem.2015.08.095
  • Šic Žlabur J, Dobričević N, Brnčić M, Barba FJ, Lorenzo JM et al. (2019). Evaluation of the behavior of phenolic compounds and steviol glycosides of sonicated strawberry juice sweetened with Stevia (Stevia rebaudiana Bertoni). Molecules 24 (7): 1202. doi: 10.3390/molecules24071202
  • Sida-Arreola JP, Sánchez E, Preciado-Rangel P, Márquez-Quiroz C (2017). Does zinc biofortification affects the antioxidant activity in common bean? Cogent Food & Agriculture 3 (1): 1283725. doi: 10.1080/23311932.2017.1283725
  • Singleton VL, Orthofer R, Lamuela-Raventós RM (1999). Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods in Enzymology 299 (1): 152-178. doi: 10.1016/S0076-6879(99)99017-1
  • Song C-Z, Liu M-Y, Meng J-F, Chi M, Xi Z-M et al. (2015). Promoting effect of foliage sprayed zinc sulfate on accumulation of sugar and phenolics in berries of Vitis vinifera cv. Merlot growing on zinc deficient soil. Molecules 20 (2): 2536-2554. doi: 10.3390/ molecules20022536
  • Tavallali V, Rahmati S, Bahmanzadegan A (2017). Antioxidant activity, polyphenolic contents and essential oil composition of Pimpinella anisum L. as affected by zinc fertilizer. Journal of the Science of Food and Agriculture 97 (14): 4883-4889. doi: 10.1002/jsfa.8360
  • Tiwari BK, OʼDonnell CP, Patras A, Cullen PJ (2008). Anthocyanin and ascorbic acid degradation in sonicated strawberry juice. Journal of Agricultural and Food Chemistry 56 (21): 10071- 10077. doi: 10.1021/jf801824v
  • Trejo-Téllez L, Gómez-Merino F (2014). Nutrient management in strawberry: effects on yield, quality and plant health. In: Malone N (editor). Strawberries: Cultivation, Antioxidant Properties and Health Benefits. New York, USA: Nova Science Publishers, Inc.
  • Van de Mortel, JE, Almar VillanuevaL, Schat H, Kwekkeboom J, Coughlan S et al. (2006). Large expression differences in genes for iron and zinc homeostasis, stress response, and lignin biosynthesis distinguish roots of Arabidopsis thaliana and the related metal hyperaccumulator Thlaspi caerulescens. Plant Physiology 142 (3): 1128-1147. doi: 10.1104/pp.106.082073
  • Vinceković M, Jalšenjak N, Topolovec-Pintarić S, Đermić E, Bujan M et al. (2016). Encapsulation of biological and chemical agents for plant nutrition and protection: Chitosan/Alginate microcapsules loaded with copper cations and Trichoderma viride. Journal of Agricultural and Food Chemistry 64 (43): 8073-8083. doi: 10.1021/acs.jafc.6b02879
  • Vinceković M, Jurić S, Đermić E, Topolovec-Pintarić S (2017a). Kinetics and mechanisms of chemical and biological agents release from biopolymeric microcapsules. Journal of Agricultural and Food Chemistry 65 (44): 9608-9617. doi: 10.1021/acs.jafc.7b04075
  • Vinceković M, Maslov Bandić L, Jurić S, Jalšenjak N, Čaić A et al. (2019). The Enhancement of bioactive potential in Vitis vinifera leaves by application of microspheres loaded with biological and chemical agents. Journal of Plant Nutrition 42 (6): 543- 558. doi: 10.1080/01904167.2019.1568467
  • Vinceković M, Topolovec Pintarić S, Jurić S, Viskić M, Jalšenjak N et al. (2017b). Release of Trichoderma viride spores from microcapsules simultaneously loaded with chemical and biological agents. Agriculturae Conspectus Scientificus 82 (4): 395-401.
  • Wang H, Jin J-Y (2007). Effects of zinc deficiency and drought on plant growth and metabolism of reactive oxygen species in maize (Zea mays L.). Agricultural Sciences in China 6 (8): 988- 995. doi: 10.1016/S1671-2927(07)60138-2
  • Yu Q, Osborne L, Rengel Z (1998). Micronutrient deficiency changes activities of superoxide dismutase and ascorbate peroxidase in tobacco plants. Journal of Plant Nutrition 21 (7): 1427-1437. doi: 10.1080/01904169809365493
Turkish Journal of Agriculture and Forestry-Cover
  • ISSN: 1300-011X
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
Sayıdaki Diğer Makaleler

Rapid and efficient in vitro regeneration of transplastomic potato (Solanum tuberosum L.) plants after particle bombardment

Emre AKSOY, Allah BAKHSH, Md Jakir HOSSAIN, Neslihan Zahide ÖZTÜRK GÖKÇE, Faiz Ahmad JOYIA, Muhammad Sarwar KHAN

Evaluation of powdery mildew resistance of a diverse set of grape cultivars and testing the association between powdery mildew resistance and PR gene expression

Semih TANGOLAR, Serpil TANGOLAR, Sinem DEMİREL AŞÇI, Kemal KAZAN, Canan YÜKSEL ÖZMEN, Mert ÖKTEM, Umut KİBAR, Muhammad MUJTABA, Ali ERGÜL

Differences of flavonoid structural genes preferentially expressed in brown and green natural colored cotton

Öner CANAVAR, Mark D. RAUSHER

Hydropriming associated physiological and biochemical changes responsible for the enhanced planting value of maize hybrid and its parental line seeds

Heena Rasool MIR, Shiv Kumar YADAV, Sangita YADAV

Determination of the in vitro bioaccessibility of phenolic compounds and antioxidant capacity of Juniper berry (Juniperus drupacea Labill.) pekmez

Osman SAĞDIÇ, Kübra ÖZKAN, Ayşe KARADAĞ

Development of a mobile robot-based combined sensor platform to determine the correlation between soil penetration resistance and electrical conductivity

Mehmet TOPAKCI, Erdem YILMAZ, İlker ÜNAL, Davut KARAYEL, Murad ÇANAKCI, Önder KABAŞ

Effects of melatonin applications on certain biochemical characteristics of strawberry seedlings in lime stress conditions

Gülden BALCI

Genetic diversity for agro-morphological characters and nutritional compositions of some local faba bean (Vicia faba L.) genotypes

Tolga KARAKÖY, Aybegün TON, Meltem TÜRKERİ, Adem Emin ANLARSAL

Stimulation of plant secondary metabolites synthesis in soilless cultivated strawberries (Fragaria × ananassa Duchesne) using zinc-alginate microparticles

Slaven JURIĆ, Kristina VLAHOVIČEK-KAHLINA, Boris DURALIJA, Luna MASLOV BANDIĆ, Petra NEKIĆ, Marko VINCEKOVIĆ

The comparison of botanical composition and the condition and health class of different rangeland sites in forest ecosystem

Emre ÇOMAKLI, M. Kerim GÜLLAP, Adnan BİLGİLİ, Tuğba ÇOMAKLI