Skip to main content
SpringerLink
Log in

Changes in phenolic acids, flavonoids, anthocyanins, and antioxidant activities of Mahonia aquifolium berries during fruit development and elucidation of the phenolic biosynthetic pathway

  • Research Report
  • Published:
Horticulture, Environment, and Biotechnology Aims and scope Submit manuscript

Abstract

It is important to determine the most suitable ripening period of fruit regarding bioactive compounds for evaluating as an industrial and in human nutrition. The aims of this study were to determine the changes in non-anthocyanin phenolics, anthocyanins, and antioxidant activity of Mahonia aquifolium fruit throughout ripening and to determine the biosynthetic pathway of the phenolic compounds. The fruit was collected from shrubs at 10 different ripening stages between June 21 and August 17, 2016. The samples were analyzed for individual anthocyanins, non-anthocyanin phenolics, and antioxidant activity. There were significant decreases in gentisic, chlorogenic, p-coumaric, ferulic acids, rutin, and isorhamnetin 3-O-glucoside and increases in protocatechuic, syringic acid, caffeic acid, myricetin, and luteolin. The concentrations of delphinidin-3-O-glucoside, cyanidin-3-O-glucoside, and pelargonidin-3-O-glucoside rose progressively from the beginning to the end of ripening, while decreases occurred from the 6th stage in the amounts of malvidin-3-O-glucoside, peonidin-3-O-glucoside, cyanidin-3-O-rutinoside, and delphinidin-3-O-rutinoside. A decrease followed by an increase in the antioxidant activity indicated that the phenolic profile of the fruit changed toward the end of ripening, including for the compounds with higher antioxidant potential. In this study, the most suitable harvesting period for Mahonia berries was determined

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Alberti A, Zielinski AAF, Couto M, Judacewski P, Mafra LI, Nogueira A (2017) Distribution of phenolic compounds and antioxidant capacity in apples tissues during ripening. J Food Sci Technol 6:1511–1518

    Article  Google Scholar 

  • Aseel DG, Rashad YM, Hammad SM (2019) Arbuscular Mycorrhizal fungi trigger transcriptional expression of flavonoid and chlorogenic acid biosynthetic pathways genes in tomato against tomato mosaic virus. Sci Rep 1:1–10

    Google Scholar 

  • Belwal T, Pandey A, Bhatt ID, Rawal RS, Luo Z (2019) Trends of polyphenolics and anthocyanins accumulation along ripening stages of wild edible fruits of Indian Himalayan region. Sci Rep 1:5894

    Article  Google Scholar 

  • Benzie IF, Strain J (1999) 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. In: Packer L (ed) Methods in enzymology. Elsevier, San Diego, pp 15–27

    Google Scholar 

  • Biała W, Jasiński M (2018) The Phenylpropanoid case—it is transport that matters. Front Plant Sci 9:1–9

    Article  Google Scholar 

  • Brand-Williams W, Cuvelier ME, Berset C (1995) Use of a free-radical method to evaluate antioxidant activity. Lebenson Wiss Technol 1:25–30

    Article  Google Scholar 

  • Butkhup L, Samappito S (2011) Changes in physico-chemical properties, polyphenol compounds and antiradical activity during development and ripening of maoluang (Antidesma bunius L. Spreng) fruits. J Fruit Ornam Plant Res 1:85–99

    Google Scholar 

  • Cao G, Sofic E, Prior RL (1997) Antioxidant and prooxidant behavior of flavonoids: structure-activity relationships. Free Radic Biol Med 5:749–760

    Article  Google Scholar 

  • Casañal A, Zander U, Muñoz C, Dupeux F, Luque I, Botella MA et al (2013) The strawberry pathogenesis-related 10 (PR-10) Fra a proteins control flavonoid biosynthesis by binding to metabolic intermediates. J Biol Chem 49:35322–35332

    Article  Google Scholar 

  • Celli GB, Pereira-Netto AB, Beta T (2011) Comparative analysis of total phenolic content, antioxidant activity, and flavonoids profile of fruits from two varieties of Brazilian cherry (Eugenia uniflora L.) throughout the fruit developmental stages. Food Res Int 8:2442–2451

    Article  Google Scholar 

  • Chaves-Silva S, dos Santos AL, Chalfun-Júnior A, Zhao J, Peres LE, Benedito VA (2018) Understanding the genetic regulation of anthocyanin biosynthesis in plants—tools for breeding purple varieties of fruits and vegetables. Phytochemistry 153:11–27

    Article  CAS  Google Scholar 

  • Coklar H, Akbulut M (2017) Anthocyanins and phenolic compounds of Mahonia aquifolium berries and their contributions to antioxidant activity. J Funct Foods 35:166–174

    Article  CAS  Google Scholar 

  • Craft BD, Kerrihard AL, Amarowicz R, Pegg RB (2012) Phenol-based antioxidants and the in vitro methods used for their assessment. Compr Rev Food Sci 2:148–173

    Article  Google Scholar 

  • de Simón BF, Hernández T, Estrella I (1992) Relationship between chemical structure and biosynthesis and accumulation of certain phenolic compounds in grape skins during ripening. Z Lebensm Unters Forsch 2:124–128

    Article  Google Scholar 

  • Deng Y, Lu S (2017) Biosynthesis and regulation of phenylpropanoids in plants. Crit Rev Plant Sci 4:257–290

    Article  Google Scholar 

  • Dong T, Han R, Yu J, Zhu M, Zhang Y, Gong Y et al (2019) Anthocyanins accumulation and molecular analysis of correlated genes by metabolome and transcriptome in green and purple asparaguses (Asparagus officinalis, L.). Food Chem 271:18–28

    Article  CAS  Google Scholar 

  • El Sayed Bashandy H (2016) Flavonoid Metabolomics in Gerbera hybrida and Elucidation of Complexity in the Flavonoid Biosynthetic Pathway (2016). https://helda.helsinki.fi/bitstream/handle/10138/159523/flavonoi.pdf?sequence=1. Accessed 09 September 2019

  • Falcone Ferreyra ML, Rius S, Casati P (2012) Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 3:222

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gibson L, Rupasinghe H, Forney C, Eaton L (2013) Characterization of changes in polyphenols, antioxidant capacity and physico-chemical parameters during lowbush blueberry fruit ripening. Antioxidants 4:216–229

    Article  Google Scholar 

  • Gutha LR, Casassa LF, Harbertson JF, Naidu RA (2010) Modulation of flavonoid biosynthetic pathway genes and anthocyanins due to virus infection in grapevine (Vitis vinifera L.) leaves. BMC Plant Biol 1:187

    Article  Google Scholar 

  • Heo HJ, Kim YJ, Chung D, Kim D-O (2007) Antioxidant capacities of individual and combined phenolics in a model system. Food Chem 1:87–92

    Article  Google Scholar 

  • Jaakola L (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trend Plant Sci 9:477–483

    Article  Google Scholar 

  • Jordão A, Da Silva JR, Laureano O (2015) Evolution of anthocyanins during grape maturation of two varieties (Vitis vinifera L.). Castelao Frances Touriga Francesa Vitis 2:93–94

    Google Scholar 

  • MSTAT Development Team (1989) MSTAT user’s guide: a microcomputer program for the design management and analysis of agronomic research experiments. Michigan State University, East Lansing, MI

    Google Scholar 

  • Meighani H, Ghasemnezhad M, Bakhshi D (2017) An evaluation of the phytochemical properties of some pomegranate cultivars during fruit development and ripening. Int J Hortic 2:193–204

    Google Scholar 

  • Murakami M, Yamaguchi T, Takamura H, Matoba T (2003) Effects of ascorbic acid and α-tocopherol on antioxidant activity of polyphenolic compounds. J Food Sci 5:1622–1625

    Article  Google Scholar 

  • Prasanna V, Prabha T, Tharanathan R (2007) Fruit ripening phenomena—an overview. Crit Rev Food Sci Nutr 1:1–19

    Article  Google Scholar 

  • Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans C (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 9–10:1231–1237

    Article  Google Scholar 

  • Rehman RNU, You YH, Ali S, Wang YL, Zhang L, Li PM et al (2018) Phenolic compounds as biochemical markers of senescence in woody ornamental flowers of Malus crabapple. Hortic Environ Biotechnol 1:1–10

    Article  Google Scholar 

  • Ribera A, Reyes-Diaz M, Alberdi M, Zuñiga G, Mora M (2010) Antioxidant compounds in skin and pulp of fruits change among genotypes and maturity stages in highbush blueberry (Vaccinium corymbosum L.) grown in southern Chile. J Soil Sci Plant Nutr 4:509–536

    Article  Google Scholar 

  • Rice-Evans CA, Miller NJ, Paganga G (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 7:933–956

    Article  Google Scholar 

  • Rice-Evans C, Miller N, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends Plant Sci 4:152–159

    Article  Google Scholar 

  • Shahidi F, Ambigaipalan P (2015) Phenolics and polyphenolics in foods, beverages and spices: Antioxidant activity and health effects—a review. J Funct Foods 18:820–897

    Article  CAS  Google Scholar 

  • Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B (2019) Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules 13:2452

    Article  Google Scholar 

  • Somani SJ, Modi KP, Majumdar AS, Sadarani BN (2015) Phytochemicals and their potential usefulness in inflammatory bowel disease. Phytother Res 3:339–350

    Article  Google Scholar 

  • Soobrattee MA, Neergheen VS, Luximon-Ramma A, Aruoma OI, Bahorun T (2005) Phenolics as potential antioxidant therapeutic agents: mechanism and actions. Mutat Res Fund Mol Mech Mut 1–2:200–213

    Article  Google Scholar 

  • Yeh C-T, Yen G-C (2003) Effects of phenolic acids on human phenolsulfotransferases in relation to their antioxidant activity. J Agric Food Chem 5:1474–1479

    Article  Google Scholar 

  • Yin R, Messner B, Faus-Kessler T, Hoffmann T, Schwab W, Hajirezaei M-R et al (2012) Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation. J Exp Bot 7:2465–2478

    Article  Google Scholar 

Download references

Acknowledgements

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Food Engineering, Selcuk University, Selcuklu, 42031, Konya, Turkey

    Hacer Coklar & Mehmet Akbulut

Authors
  1. Hacer Coklar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mehmet Akbulut
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Hacer Coklar and Mehmet Akbulut performed the experiments, developing the methodology and preparing the manuscript and laboratory studies.

Corresponding author

Correspondence to Mehmet Akbulut.

Ethics declarations

Conflict of interest

The authors declare that they have no confict of interest.

Additional information

Communicated by Ali Sarkhosh.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Coklar, H., Akbulut, M. Changes in phenolic acids, flavonoids, anthocyanins, and antioxidant activities of Mahonia aquifolium berries during fruit development and elucidation of the phenolic biosynthetic pathway. Hortic. Environ. Biotechnol. 62, 785–794 (2021). https://doi.org/10.1007/s13580-021-00348-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13580-021-00348-9

Keywords

Search

Navigation