Temporal, Plant Part, and Interpopulation Variability of Secondary Metabolites and Antioxidant Activity of Inula helenium L.
Abstract
:1. Introduction
2. Results
2.1. Concentration of Total Phenolic Compounds
2.2. Concentration of Flavonoids
2.3. Antioxidant Activity
2.4. Correlation Coefficient
3. Discussion
4. Materials and Methods
4.1. Plant Material
4.2. Preparation of Plant Extracts
4.3. Determination of Total Phenolics in the Plant Extracts
4.4. Determination of Total Flavonoids in the Plant Extracts
4.5. Evaluation of Antioxidant Activity
4.6. Statistical Analysis
5. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Bourgaud, F.; Gravot, A.; Milesi, S.; Gontier, E. Production of plant secondary metabolites: A historical perspective. Plant Sci. 2001, 161, 839–851. [Google Scholar] [CrossRef]
- Jakovljević, D.; Stanković, M.; Bojović, B.; Topuzović, M. Regulation of early growth and antioxidant defense mechanism of sweet basil seedlings in response to nutrition. Acta Physiol. Plant. 2017, 39, 243. [Google Scholar] [CrossRef]
- Oh, M.M.; Trick, H.N.; Rajasheka, C.B. Secondary metabolism and antioxidants are involved in environmental adaptation and stress tolerance in lettuce. J. Plant Physiol. 2009, 166, 180–191. [Google Scholar] [CrossRef] [PubMed]
- Ramakrishna, A.; Ravishankar, G.A. Influence of abiotic stress signals on secondary metabolites in plants. Plant Signal. Behav. 2011, 6, 1720–1731. [Google Scholar] [PubMed]
- Larbat, R.; Paris, C.; Le Bot, J.; Adamowicz, S. Phenolic characterization and variability in leaves, stems and roots of Micro-Tom and patio tomatoes, in response to nitrogen limitation. Plant Sci. 2014, 224, 62–73. [Google Scholar] [CrossRef] [PubMed]
- Khan, F.; Niaz, K.; Maqbool, F.; Ismail Hassan, F.; Abdollahi, M.; Nagulapalli Venkata, K.C.; Nabavi, S.M.; Bishayee, A. Molecular targets underlying the anticancer effects of quercetin: An update. Nutrients 2016, 8, 529. [Google Scholar] [CrossRef] [PubMed]
- Deriu, A.; Zanetti, S.; Sechi, L.A.; Marongiu, B.; Piras, A.; Porcedda, S.; Tuveri, E. Antimicrobial activity of Inula helenium L. essential oil against Gram-positive and Gram-negative bacteria and Candida spp. Int. J. Antimicrob. Agents 2008, 31, 588–590. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Ni, Z.Y.; Zhu, M.C.; Dong, M.; Wang, S.M.; Shi, Q.W.; Zhang, M.L.; Wang, Y.F.; Huo, C.H.; Kjyota, H.; et al. Antitumour activities of sesquiterpene lactones from Inula helenium and Inula japonica. Z. Naturfrosch. C 2012, 67, 375–380. [Google Scholar] [CrossRef]
- Kumar, S.; Pandey, A.K. Chemistry and biological activities of flavonoids: An overview. Sci. World J. 2013, 2013, 16. [Google Scholar] [CrossRef]
- Filipović, V.; Jevdjović, R.; Glamočlija, D.; Jovanović, B. Possibility of growing elecampane in conditions of non-watering field crop production. J. Agric. Sci. 2005, 50, 1–8. [Google Scholar] [CrossRef]
- Mamedov, N.; Mehdiyeva, N.P.; Craker, E.L. Medicinal plants used in traditional medicine of the Caucasus and North America. J. Med. Act. Plants 2015, 4, 42–66. [Google Scholar]
- Zhao, T.M.; Zhang, M.L.; Shi, Q.U.; Kiyota, H. Chemical constituents of plants from the genus Inula. Chem. Biodiv. 2006, 3, 371–384. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Zhao, M.Y.; Guo, Y.C.; Zhang, M.S.; Liu, L.C.; Zhang, D.S.; Bai, X.M. Ultrasound-assisted extraction of total flavonoids from Inula helenium. Pharmacogn. Mag. 2012, 8, 166–170. [Google Scholar]
- Afemei, M.; Gille, E.; Boz, I.; Toma, C.; Zamfirache, M.M. Aspects regarding the qualitative and quantitative phytochemical analysis of the Inula helenium L. species. Biologie vegetală 2012, 58, 29–34. [Google Scholar]
- Wojdyło, A.; Oszmiański, J.; Czemerys, R. Antioxidant activity and phenolic compounds in 32 selected herbs. Food Chem. 2007, 105, 940–949. [Google Scholar] [CrossRef]
- Spiridon, I.; Nechita, B.C.; Niculaua, M.; Silion, M.; Armatu, A.; Teaca, C.A.; Bodirlau, R. Antioxidant and chemical properties of Inula helenium root extracts. Cent. Eur. J. Chem. 2013, 11, 1699–1709. [Google Scholar] [CrossRef]
- Zhou, K.; Yu, L. Effects of extraction solvent on wheat bran antioxidant activity estimation. LWT Food Sci. Technol. 2004, 37, 717–721. [Google Scholar] [CrossRef]
- Shi, J.; Nawaz, H.; Pohorly, J.; Mittal, G.; Kakuda, Y.; Jiang, Y. Extraction of polyphenolics from plant material for functional foods-engeneering and technology. Food Rev. Int. 2005, 21, 139–166. [Google Scholar] [CrossRef]
- Naidoo, Y.; Sadashiva, T.C.; Raghu, K. Antibacterial, antioxidant and phytochemical properties of the ethanolic extract of Ocimum obovatum E.Mey ex Benth. Indian J. Tradit. Knowl. 2016, 15, 57–61. [Google Scholar]
- Kliebenstein, D.J.; Osbourn, A. Making new molecules—evolution of pathways for novel metabolites in plants. Curr. Opin. Plant Biol. 2012, 15, 415–423. [Google Scholar] [CrossRef]
- Alonso-Amelot, M.E.; Oliveros-Bastidas, A.; Calcagno-Pisarelli, M.P. Phenolics and condensed tannins in relation to altitude in neotropical Pteridium spp. A field study in the Venezuelan Andes. Biochem. Syst. Ecol. 2004, 32, 969–981. [Google Scholar] [CrossRef]
- Li, Y.; Gao, J.; Zhang, L.; Su, Z. Responses to UV-B exposure by saplings of the relict species Davidia involucrata Bill are modified by soil nitrogen availability. Pol. J. Ecol. 2014, 62, 101–110. [Google Scholar] [CrossRef]
- Alonso-Amelot, M.E.; Oliveros-Bastidas, A.; Calcagno-Pisarelli, M.P. Phenolics and condensed tannins of high altitude Pteridium arachnoideum in relation to sunlight exposure, elevation, and rain regime. Biochem. Syst. Ecol. 2007, 35, 1–10. [Google Scholar] [CrossRef]
- Binder, B.Y.; Peebles, C.A.; Shanks, J.V.; San, K.Y. The effects of UV-B stress on the production of terpenoid indole alkaloids in Catharanthus roseus hairy roots. Biotechnol. Prog. 2011, 25, 861–865. [Google Scholar] [CrossRef] [PubMed]
- Maoulainine, L.B.M.; Jelassi, A.; Hassen, I.; Boukhari, A.O.M.S.O. Antioxidant properties of methanolic and ethanolic extracts of Euphorbia helioscopia L. aerial parts. Int. Food Res. J. 2012, 19, 1125–1130. [Google Scholar]
- Bystricka, J.; Vollmannova, A.; Margitanova, E.; Cicova, I. Dynamics of polyphenolics formation in different plant parts and different growth phases of selected buckwheat cultivars. Acta Agric. Slov. 2010, 95, 225–229. [Google Scholar] [CrossRef]
- Erturk, Y.; Ercisli, S.; Şengül, M.; Eser, Z.; Haznedear, A.; Turan, M. Seasonal variation of total phenolic, antioxidant activity and minerals in fresh tea shoots (Camellia sinensis var. sinensis). Pak. J. Pharm. Sci. 2010, 23, 69–74. [Google Scholar]
- Jabłońska, K.; Kwiatkowska-Falińska, A.; Czernecki, B.; Walawender, P.J. Changes in spring and summer phenology in Poland—responses of selected plant species to air temperature variations. Pol. J. Ecol. 2015, 63, 311–319. [Google Scholar] [CrossRef]
- Liu, L.; Gitz, C.D.; McClure, W.J. Effects of UV-B on flavonoids, ferulic acid, growth and photosynthesis in barley primary leaves. Physiol. Plant 1995, 93, 725–733. [Google Scholar] [CrossRef]
- Barros, L.; Carvalho, A.M.; Ferreira, C.F.R. Comparing the composition and bioactivity of Crataegus monogyna flowers and fruits used in folk medicine. Phytochem. Anal. 2011, 22, 181–188. [Google Scholar] [CrossRef]
- Riahi, L.; Chograni, H.; Elferchichi, M.; Zaouali, Y.; Zoghlami, N.; Mliki, A. Variations in Tunisian wormwood essential oil profiles and phenolic contents between leaves and flowers and their effects on antioxidant activities. Ind. Crop. Prod. 2013, 46, 290–296. [Google Scholar] [CrossRef]
- Kołodziejek, J.; Michlewska, S. Effect of soil moisture on morpho-anatomical leaf traits of Ranunculus acris (Ranunculaceae). Pol. J. Ecol. 2015, 63, 400–413. [Google Scholar] [CrossRef]
- Papageorgiou, V.; Gardeli, C.; Mallouchos, A.; Papaioannou, M.; Komaitis, M. Variation of the chemical profile and antioxidant behavior of Rosmarinus officinalis L. and Salvia fruticosa Miller grown in Greece. J. Agric. Food Chem. 2008, 56, 7254–7264. [Google Scholar] [CrossRef]
- Ganzera, M.; Guggenberger, M.; Stuppner, H.; Zidorn, C. Altitudinal variation of secondary metabolite profiles in flowering heads of Matricaria chamomilla cv. BONA. Planta Med. 2008, 74, 453–457. [Google Scholar] [CrossRef] [PubMed]
- Talib, H.W.; Mahasneh, M.A. Antiproliferative activity of plant extracts used against cancer in traditional medicine. Sci. Pharm. 2018, 78, 33–45. [Google Scholar] [CrossRef] [PubMed]
- Ksouri, R.; Megdiche, W.; Falleh, H.; Trabelsi, N.; Boulaaba, M.; Smaoui, A.; Abdelly, C. Influence of biological, environmental and technical factors on phenolic content and antioxidant activities of Tunisian halophytes. C. R. Biol. 2008, 331, 865–873. [Google Scholar] [CrossRef]
- Tosun, M.; Ercisli, S.; Sengul, M.; Ozer, H.; Polat, T. Antioxidant properties and total phenolic content of eight Salvia species from Turkey. Biol. Res. 2009, 42, 175–181. [Google Scholar] [CrossRef]
- Stanković, M.S.; Topuzović, M.; Solujić, S.; Mihailović, V. Antioxidant activity and concentration of phenols and flavonoids in the whole plant and plant parts of Teucrium chamaedrys L. var. glanduliferum Haussk. J. Med. Plants Res. 2010, 4, 2092–2098. [Google Scholar]
- Stanković, M.S.; Nićiforović, N.; Topuzović, M.; Solujić, S. Total phenolic content, flavonoid concentrations and antioxidant activity, of the whole plant and plant parts extracts from Teucrium montanum L. var. montanum, f. supinum (L.) Reichenb. Biotechnol. Biotechnol. Equip. 2011, 25, 2222–2227. [Google Scholar] [CrossRef]
- Alías, J.C.; Sosa, T.; Valares, C.; Escudero, J.C.; Chaves, N. Seasonal variation of Cistus ladanifer L. diterpenes. Plants 2012, 1, 6–15. [Google Scholar] [CrossRef]
- Valares Masa, C.; Sosa Díaz, T.; Alías Gallego, J.C.; Chaves Lobón, N. Quantitative Variation of Flavonoids and Diterpenes in Leaves and Stems of Cistus ladanifer L. at Different Ages. Molecules 2016, 21, 275. [Google Scholar] [CrossRef] [PubMed]
- Valares Masa, C.; Alías Gallego, J.C.; Chaves Lobón, N.; Sosa Díaz, T. Intra-Population Variation of Secondary Metabolites in Cistus ladanifer L. Molecules 2016, 21, 945. [Google Scholar] [CrossRef] [PubMed]
- Petkova, N.; Ivanov, I.; Vrancheva, R.; Denev, P.; Pavlov, A. Ultrasound and microwave-assisted extraction of elecampane (Inula helenium) roots. Nat. Prod. Commun. 2017, 12, 171–174. [Google Scholar] [CrossRef] [PubMed]
- Park, E.J.; Kim, Y.M.; Park, S.W.; Kim, H.J.; Lee, J.H.; Lee, D.U.; Chang, K.C. Induction of HO-1 through p38 MAPK/Nrf2 signaling pathway by ethanol extract of Inula helenium L. reduces inflammation in LPS-activated RAW 264.7 cells and CLP-induced septic mice. Food Chem. Toxicol. 2013, 55, 386–395. [Google Scholar] [CrossRef] [PubMed]
- Singleton, V.L.; Orthofer, R.; Lamuela, R.R.M. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 1991, 299, 152–178. [Google Scholar]
- Quettier, D.C.; Gressier, B.; Vasseur, J.; Dine, T.; Brunet, C.; Luyckx, M.; Cazin, M.; Cazin, J.C.; Bailleul, F.; Trotin, F. Phenolic compounds and antioxidant activities of buckwheat (Fagopyrum esculentum Moench) hulls and flour. J. Ethnopharmacol. 2000, 72, 35–42. [Google Scholar] [CrossRef]
- Takao, T.; Watanabe, N.; Yagi, I.; Sakata, K. A simple screeninig method for antioxidant and isolation of several antioxidants produced by marine bacteria from fish and shellfish. Biosci. Biotechnol. Biochem. 1994, 58, 1780–1783. [Google Scholar] [CrossRef]
Locality | Root | Stem | Leaves | Inflorescence | p |
---|---|---|---|---|---|
Locality 1a | 71.24 ± 0.49 | 27.43 ± 0.12 | 69.02 ± 0.51 | 89.85 ± 1.38 | a |
Locality 1b | 67.22 ± 0.80 | 26.35 ± 0.25 | 67.08 ± 0.69 | 88.60 ± 1.27 | a |
Locality 2 | 44.40 ± 1.18 | 16.73 ± 0.18 | 49.61 ± 1.04 | 61.06 ± 0.57 | b * |
Locality | Root | Stem | Leaves | Inflorescence | p |
---|---|---|---|---|---|
Locality 1a | 20.27 ± 0.29 | 66.88 ± 0.39 | 376.22 ± 2.88 | 41.47 ± 1.61 | a |
Locality 1b | 12.56 ± 0.19 | 29.01 ± 0.37 | 250.86 ± 3.35 | 38.23 ± 0.33 | ab |
Locality 2 | 9.32 ± 0.21 | 20.04 ± 0.61 | 191.20 ± 1.25 | 25.42 ± 0.56 | b |
Locality | Root | Stem | Leaves | Inflorescence | p |
---|---|---|---|---|---|
Locality 1a | 161.60 ± 2.11 | 619.73 ± 3.05 | 338.83 ± 2.95 | 183.95 ± 1.51 | a |
Locality 1b | 198.01 ± 1.84 | 842.05 ± 4.16 | 573.82 ± 3.12 | 222.25 ± 1.92 | a |
Locality 2 | 285.10 ± 2.35 | 1563.02 ± 6.77 | 865.32 ± 4.88 | 427.35 ± 2.08 | b * |
Plant Parts | ||||
TP | TF | AA | ||
Root | TP | 1 | 0.816 | −0.988 |
TF | - | 1 | −0.894 | |
AA | - | - | 1 | |
Stem | TP | 1 | 0.715 | −0.990 |
TF | - | 1 | −0.803 | |
AA | - | - | 1 | |
Leaves | TP | 1 | 0.805 | −0.932 |
TF | - | 1 | −0.965 | |
AA | - | - | 1 | |
Inflorescence | TP | 1 | 0.988 | −0.994 |
TF | - | 1 | −0.998 | |
AA | - | 1 | ||
Localities | ||||
TP | TF | AA | ||
Locality 1a | TP | 1 | 0.035 | −0.931 |
TF | - | 1 | 0.143 | |
AA | - | - | 1 | |
Locality 1b | TP | 1 | 0.138 | −0.863 |
TF | - | 1 | 0.265 | |
AA | - | - | 1 | |
Locality 2 | TP | 1 | 0.249 | −0.834 |
TF | - | 1 | 0.114 | |
AA | - | - | 1 |
Sample | Locality | Type of Habitat/Vegetation | Altitude and Exposure | Latitude and Longitude | Date of Sampling |
---|---|---|---|---|---|
Sample 1 | Locality 1a (Bratljevo) | Mesophilous habitat, the edge of the forest | 973 m, W | 43°28′32″ N 20°10′24″ S | 12 July 2014 |
Sample 2 | Locality 1b (Bratljevo) | Mesophilous habitat, the edge of the forest | 973 m, W | 43°28′32″ N 20°10′24″ S | 19 October 2014 |
Sample 3 | Locality 2 (Prilike) | Hygrophilous habitat, forest stream bank | 447 m, W | 43°37’50" N 20°8′44″ S | 12 July 2014 |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Zlatić, N.; Jakovljević, D.; Stanković, M. Temporal, Plant Part, and Interpopulation Variability of Secondary Metabolites and Antioxidant Activity of Inula helenium L. Plants 2019, 8, 179. https://doi.org/10.3390/plants8060179
Zlatić N, Jakovljević D, Stanković M. Temporal, Plant Part, and Interpopulation Variability of Secondary Metabolites and Antioxidant Activity of Inula helenium L. Plants. 2019; 8(6):179. https://doi.org/10.3390/plants8060179
Chicago/Turabian StyleZlatić, Nenad, Dragana Jakovljević, and Milan Stanković. 2019. "Temporal, Plant Part, and Interpopulation Variability of Secondary Metabolites and Antioxidant Activity of Inula helenium L." Plants 8, no. 6: 179. https://doi.org/10.3390/plants8060179