Skip to main content
Download PDF

Antioxidant and tyrosinase inhibition activity of the fertile fronds and rhizomes of three different Drynaria species

BMC Research Notes volume 8, Article number: 468 (2015) Cite this article

Abstract

Background

For generations, the rhizomes of Drynaria ferns have been used as traditional medicine in Asia. Despite this, the bioactivities of Drynaria rhizomes and leaves have rarely been studied scientifically.

Methods

This study evaluates the antioxidant properties of the methanolic extracts of the fertile fronds and rhizomes from three species in this genus: Drynaria quercifolia, Drynaria rigidula and Drynaria sparsisora. The phenolic and flavonoid contents of the samples were respectively quantified with the total phenolic content (TPC) and total flavonoid content (TFC) assays, while the antioxidant activities were determined via measuring the DPPH radical scavenging activity (FRS), ferric reducing power (FRP), ferrous ion chelating (FIC) activity and lipid peroxidation inhibition (LPI). The tyrosinase inhibition activity of all three species was also reported.

Results

The fertile fronds of D. quercifolia were found to exhibit the highest overall TPC (2939 ± 469 mg GAE/100 g) and antioxidant activity amongst all the samples, and the fertile fronds of D. quercifolia and D. rigidula exhibited superior TPC and FRP compared to their rhizomes, despite only the latter being widely used in traditional medicine. The fronds of D. quercifolia had high tyrosinase inhibition activity (56.6 ± 5.0 %), but most of the Drynaria extracts showed unexpected tyrosinase enhancement instead, particularly for D. sparsisora’s fronds.

Conclusion

The high bioactivity of the fertile fronds in the fern species indicate that there is value in further research on the fronds of ferns which are commonly used mostly, or only, for their rhizomes.

Background

Interest in phenolic compounds has been on the rise due to their potential human health benefits [1]. They are the most abundant class of plant antioxidants—compounds capable of deactivating or stabilizing free radicals, thereby reducing free-radical-mediated cellular and tissue damage [2]. Plant antioxidants have been purported to have anti-aging properties, and may prevent numerous diseases such as cancer, diabetes, neurodegenerative diseases [3], atherosclerosis, and cardiovascular diseases [4]. Some phenolic compounds are also able to inhibit tyrosinase, an enzyme responsible in melanogenesis and enzymatic browning. This has considerable commercial value in the cosmetics industry as a skin-whitening agent, or an anti-browning agent in the food industry [5]. Tyrosinase inhibition has also been discovered to reduce the viability of catecholaminergic neuronal cells [6] which have been linked to several psychiatric and neurodegenerative disorders, thus providing a possible new treatment in the future [7].

The rhizomes of the Drynaria genus of ferns have a long history of being used as traditional medicine, particularly in India [8], China [9] and Southeast Asia [10]. Drynaria quercifolia (L.) J. Smith is one of the best-known members of this genus, commonly used in Ayurvedic medicine (“Ashwakatri”) [8] where its boiled rhizome decoction is consumed orally for its anti-pyretic properties; and used as a treatment for tuberculosis [10], diarrhea, cholera, fever, typhoid, syphilis and skin diseases [11]. Additionally, the extract of this fern was capable of inhibiting wildtype and multidrug-resistant bacteria such as Neisseria gonorrhoeae and Streptococcus-β-haemolyticus [10]. Due to the ethnobotanical value of the D. quercifolia’s rhizomes, it has been the emphasis of phytochemical-centric research on the species. In comparison, little research has been conducted on the fertile fronds (leaves), which are sometimes used in conjunction with the rhizome to treat tuberculosis and throat infections [12], or as a poultice to reduce swelling [8].

The rhizomes of Drynaria rigidula (Sw.) Beddome and Drynaria sparsisora (Desv.) T. Moore have also been claimed to treat similar diseases as the rhizomes of D. quercifolia, such as diarrhea and gonorrhea [13]. However, unlike D. quercifolia, there have been no reports on the bioactivity of the fertile fronds of both species. D. rigidula is an endangered species in many locations [14], while D. sparsisora is nearly identical to D. quercifolia in physical appearance, but with shorter fertile fronds [15] and a dark-colored scaly rhizome [16]. This study represents the first time that the antioxidant activities of D. rigidula and D. sparsisora fertile fronds and rhizomes have ever been reported, and the comparison between the antioxidant activity of fertile fronds and rhizomes in a fern remains a rarely-explored avenue in most literature. This is also the first time that the tyrosinase inhibition activity for any of these species has ever been reported.

Methods

Collection of fern samples

The fertile fronds and rhizomes of D. quercifolia and D. rigidula were obtained from the Putrajaya Botanical Garden, Kuala Lumpur, while the leaves and rhizomes of D. sparsisora were obtained from Sunway, Petaling Jaya. The ferns were identified by plant taxonomist Anthonysamy S., formerly from University Putra Malaysia.

Chemicals and reagents

The various reagents used throughout this project were purchased from suppliers as follows. TPC analysis: Folin–Ciocalteu’s phenol reagent (2 N, R and M Chemicals, Essex, UK), gallic acid (98 %, Fluka, Steinheim, France), anhydrous sodium carbonate (99 %, J. Kollin, UK); total flavonoid content (TFC) analysis: aluminium chloride (99.5 %, Bendosen Laboratory Chemicals, Bendosen, Norway), potassium acetate (99 %, R and M chemicals), quercetin (98 %, Sigma St. Louis, MO, USA); diphenyl-2-picrylhydrazyl (DPPH·) assay: 1,1-diphenyl-2-picrylhydrazyl (90 %, Sigma, St. Louis, MO, USA); ferric reducing power (FRP) assay: ferric chloride hexa-hydrate (100 %, Fisher Scientific, Loughborough, UK), potassium ferricyanide (99 %, Unilab, Auburn, Australia), trichloroacetic acid (99.8 %, HmbG Chemicals, Barcelona, Spain), potassium dihydrogen orthophosphate (99.5 %, Fisher Scientific, Loughborough, UK), dipotassium hydrogen phosphate (99 %, Merck, Darmstadt, Germany), iron chloride (99 %, R&M Chemicals, Petaling Jaya, Malaysia); ferrous ion chelating (FIC) assay: ferrozine (98 %, Acros Organics, Morris Plains, NJ, USA), ferrous sulphate hepta-hydrate (HmbG Chemicals, Barcelona, Spain), ethylenediaminetetraacetic acid (EDTA) (98 %, Sigma, St. Louis, MO, USA); lipid peroxidation inhibition (LPI): β-carotene (Sigma, St. Louis, MO, USA), chloroform (Fisher Scientific, 99.9 %, Loughborough, UK), linoleic acid, C18H32O2 (Fluka, Steinheim, France), Tween 40 (Fluka, Steinheim, France); tyrosinase inhibition activity: 3, 4-dihydroxy-l-phenylalanine C9H11NO4 (Sigma, St. Louis, MO, USA), dimethyl sulfoxide analytical grade (Fisher Scientific, Loughborough, UK), kojic acid C6H6O4 (Sigma, St. Louis, MO, USA), tyrosinase (catechol oxidasemonophenol, dihydroxyphenylalanine) 3400 units/mg solid (Sigma, St. Louis, MO, USA).

Extraction of samples

Fresh fertile fronds were extracted at a ratio of 50 mL 70 % methanol to 1 g of leaf material after liquid nitrogen-aided crushing. For the rhizomes, 1.0 g of de-skinned rhizome was extracted at a ratio of 50 mL 50 % methanol to 1 g of rhizome. The methanol concentrations chosen for extraction were based on preliminary extraction efficiency screening, where 70 and 50 % methanol were found to be more efficient at extracting the fertile fronds and rhizomes respectively. The extracts were then filtered with a Buchner funnel. The methanolic extracts were stored at −20 °C when not in use.

Determination of antioxidant activity

Determination of total phenolic content (TPC)

The determination of the total phenolic content of the samples was done using a procedure modified from Kähkönen et al. [17] utilizing the Folin–Ciocalteu reagent. Samples (300 μL, in triplicate) were mixed with 1.5 mL of the 10 % Folin–Ciocalteu reagent, followed by an addition of 1.2 mL of 7.5 % (w/v) sodium carbonate (Na2CO3) solution. The test tubes were then left to stand for 30 min in the dark at room temperature before the absorbance values were measured at 765 nm. The total phenolic content was expressed as mg gallic acid equivalent per 100 g of sample (mg GAE/100 g).

Total flavonoid content (TFC)

Flavonoid content in the extract was determined with the aluminium chloride colorimetric method as described in Chang et al. [18]. Equal volumes of 10 % aluminium chloride and 1.0 M potassium acetate (0.1 mL each) were added to 0.5 mL of extract, followed by 2.8 mL of distilled water. The solutions were mixed well and incubated at room temperature for 30 min before the absorbance was taken at 415 nm. The flavonoid concentration was expressed as mg quercetin equivalent per 100 g sample, mg QE/100 g.

DPPH radical scavenging assay (FRS)

The DPPH· assay was based on the procedures described in Leong and Shui [19] and Miliauskas et al. [20] where the reduction of the DPPH (2,2-diphenyl-1-picrylhydrazyl) radical was measured spectrometrically to determine the radical scavenging activity of the extract. Two mL of DPPH· solution (5.9 mg in 100 mL methanol) was added to 1 mL of three different concentrations of the of sample extract (diluted with methanol). The absorbance of the solution was measured at 517 nm after a 30 min incubation time. The free radical scavenging activity (FRS) was expressed as ascorbic acid (AA) equivalent antioxidant capacity, in mg AA/100 g using the equation: \({\text{AEAC}} = {\text{IC}}_{{ 50({\text{AA}})}} /{\text{IC}}_{{ 50({\text{sample}})}} \; \times \; 10^{ 5}\). IC50 of AA used for calculation of FRS was 0.00387 mg/mL.

Ferric reducing power (FRP) assay

The reducing power of the extracts was determined using potassium hexacyanoferrate(III) as described in the procedure described by Tan and Chan [21]. The FRP assay was used to assess the ability of any antioxidants present in the extracts to reduce ferric ions (Fe3+) to ferrous ions (Fe2+). One mL of sample extract of different concentration (diluted with methanol) was added with 2.5 mL of 0.2 M phosphate buffer (pH 6.7) and the same volume of 1 % (w/v) potassium ferricyanide. The solutions were mixed and incubated in 50 °C water bath for 20 min. Subsequently, 2.5 mL of 10 % trichloroacetic acid was added to stop the reaction. Then, the solution in each test tube was separated into aliquots of 2.5 mL, added with 2.5 mL of Milli-Q water and 0.5 mL of 0.1 % FeCl3. The solutions were mixed and left on bench for 30 min before the absorbance was measured at 700 nm. FRP was expressed as mg gallic acid equivalent per gram of sample, mg GAE/g.

Ferrous ion chelating (FIC) assay

The determination of ferrous ion chelating strength of the extract was based on the procedures described in Mau et al. [22], and Singh and Rajini [23]. One mL of 0.1 mM FeSO4 was added to 1 mL of sample of different concentrations (0.2, 0.5 and 1 mL of extract, diluted with methanol), followed by 1 mL of 0.25 mM ferrozine. The mixtures were incubated at room temperature for 10 min before the absorbance was measured at 562 nm. It was expressed as the percentage of iron chelating activity. EDTA (0.017–0.067 mg/mL) was used as a positive control.

Lipid peroxidation inhibition (LPI)

Lipid peroxidation inhibition was adapted from Kumazawa et al. [24] based on the bleaching of β-carotene with slight modifications. Six mg of β-carotene was dissolved in 50 mL of chloroform, and 4 mL of the solution was mixed with 40 mg of linoleic acid and 400 mg of Tween 40 emulsifier in a conical flask. Nitrogen gas was then used to evaporate the chloroform. Then, 100 mL of oxygenated Milli-Q water was added and the flask was shaken for the mixture to be fully dissolved. Immediately after water was added, the absorbance of the mixture was measured at 470 and 700 nm using Perkin-Elmer double-beam spectrophotometer. Next, 3 mL of the emulsion was added into test tubes with different volume of sample (10, 50 and 100 μL). The tubes were sealed with parafilm and incubated at 50 °C water bath for an hour before the absorbance was measured again. For control, 100 μL of methanol was used instead of the sample. The blank was prepared by adding the same volume of sample with the emulsion of 400 mg Tween 40 emulsifier and 100 mL of water but without linoleic acid and β-carotene solution. The absorbance (A) at 700 nm was taken in order to correct the haze present in the solution. The LPI was calculated using the formula:

$${\text{Degradation Rate }}\left( {\text{DR}} \right) \, = \, \left[ {{\text{Ln }}\left( {{\text{A}}_{\text{Initial}} / {\text{A}}_{\text{Sample}} } \right)} \right]/ 60$$
$${\text{Antioxidant Activity }}\left( {\% {\text{ AOA}}} \right) \, = \, \left[ { 1 { }{-} \, \left( {{\text{DR}}_{\text{Sample}} / {\text{DR}}_{\text{Control}} } \right)} \right]\; \times \; 100.$$

Determination of tyrosinase inhibition activity

The measurement of tyrosinase inhibition activity of extracts was based on the method used by Masuda et al. [25], with slight modification. The method utilizes l-DOPA and a 96-well microplate for screening of multiple samples simultaneously. For testing of the sample extract, the wells in triplicate were added with 80 μL of buffer (0.1 M phosphate buffer, pH 6.8), 40 μL of tyrosinase (1 mg/mL of tyrosinase diluted 50-folds with Milli-Q water), and 40 μL of sample (1 mg of freeze-dried extract in 400 μL of 50 % DMSO), and lastly 40 μL of l-DOPA. For the control, the same reagents were added to the wells except that the sample was substituted with 40 μL of DMSO. The blank contained 120 μL of buffer, 40 μL of tyrosinase, and 40 μL of sample. The mixture in each well was mixed and left on the bench for 30 min (after the addition of l-DOPA). Subsequently, the microplate was measured using BIOTEK PowerWave XS Microplate Scanning Spectrophotometer at the absorbance of 475 nm, with reference wavelength at 700 nm. The percentage tyrosinase inhibition activity was calculated using equation below:

$$\% {\text{ Tyrosinase inhibition activity}} = \, \left[ { 1 { }{-} \, \left( {{\text{A}}_{\text{Sample}} / {\text{A}}_{\text{Control}} } \right)} \right]\; \times \; 100.$$

Statistical analysis

Statistical analysis was carried out with one-way ANOVA and the Tukey HSD test was used to identify any significance between the TPC values of the samples. p < 0.05 was considered to be significantly different.

Results and discussion

The TPC, FRS, FRP and TFC results reported in Table 1 are a measure of the primary antioxidant activity—the ability to scavenge free radicals, thus inhibiting chain initiation and terminating chain propagation [26]. D. quercifolia fertile fronds exhibited a very high TPC of 2939 ± 469 mg GAE/100 g—consistent with previous findings reported by our research group where D. quercifolia fertile fronds ranked second highest in TPC amongst the fifteen ferns screened with an average TPC exceeding 2500 mg GAE/100 g [27]. D. quercifolia had the highest TPC of the three species screened: approximately three times higher than the fronds of D. rigidula and nearly ten-fold higher than the fronds of D. sparsisora; a surprising result given the similar physical appearance of the D. quercifolia and D. sparsisora fronds. The results for the FRS activity (IC50 and AEAC) reflected a similar correlation, with D. quercifolia fronds exhibiting the highest activity, followed by D. rigidula and D. sparsisora. However, despite the higher TPC and FRS in D. rigidula fronds compared to D. sparsisora fronds, the FRP between the fronds of both species were similar thus indicating that phenolic compounds may not necessarily be the only reducing agents present in the fronds of D. sparsisora.

Table 1 Total phenolic content (TPC), free radical scavenging activity (IC50 and ascorbic acid equivalent antioxidant capacity, AEAC), ferric reducing power (FRP) and total flavonoid content (TFC) of Drynaria sp fertile fronds and rhizomes
Full size table

When compared to the fertile fronds, the rhizomes of D. quercifolia and D. rigidula exhibited lower primary antioxidant activity, with lower TPC and weaker FRP activity (Table 1). Only in D. sparsisora was there no significant difference in TPC and FRP between the leaves and rhizomes, but the rhizomes showed significantly higher FRS than the fronds. Despite the TPC of D. sparsisora’s leaves and rhizomes being comparable with one another, the free-radical scavenging capability of the rhizomes was considerably higher than would be expected based on the TPC alone. This indicates the rhizomes of D. sparsisora either contain non-phenolic free-radical scavengers, or the phenols in the rhizomes are better free radical scavengers than those in the fertile fronds. While it has been reported that the leaves of a plant may contain more phenols than the rhizomes [28, 29], this is nevertheless an interesting finding as thus far, only the rhizomes of these ferns have been used in ethnobotany.

The lipid peroxidation inhibition (LPI) activity (Fig. 1), measures the ability of an antioxidant to inhibit lipid peroxidation, thus being a more accurate assessment of the hydrophobic antioxidants present. This is in contrast to the FRS activity (Table 1) that measures the antioxidant activity of both hydrophilic and hydrophobic compounds. All three species showed considerable antioxidant activity of 50 % or above at the maximum concentration tested (645.2 μg fresh sample/mL) in a concentration-dependant manner. The LPI between the fronds and rhizomes were comparable despite the differences in other facets of their antioxidant activity (Table 1), indicating the hydrophobic antioxidants present in both the fronds and rhizomes were comparable in antioxidant activity. Examples of such hydrophobic antioxidants would include terpenoids/carotenoids and tocopherols [30].

Fig. 1
figure 1

Lipid peroxidation inhibition (LPI) of fertile fronds and rhizomes of Drynaria sp. The figure shows bars of three different colors. The blue bar represents “66.4 μg/mL”, the red bar represents “327.9 μg/mL” and the green bar represents “645.2 μg/mL”

Full size image

While the TPC, FRS, FRP, TFC and BCB assays are measures of primary antioxidant activity, ferrous ion chelating (FIC) activity is a measure of secondary antioxidant activity—the ability to prevent the formation of radicals, such as those generated by the Fenton reaction in the presence of free ferrous ions [31]. Interestingly, the fertile fronds and rhizomes of all three species showed a low ferrous ion chelating activity, with the fertile fronds of D. rigidula showing the highest chelating activity at approximately 45 % at 7 mg/mL (Fig. 2). This appears to be a common phenomena amongst ferns, as even those with exceptionally high TPC values exceeding 2500 mg GAE/100 g, such as Cyathea latebrosa, Cibotium barometz and Dicranopteris linearis, have been reported to exhibit poor chelating activity [27]. The phenolic compounds present in the Drynaria samples are likely weak iron chelators, and thus, weak secondary antioxidants.

Fig. 2
figure 2

Ferrous iron chelating (FIC) activity in fertile fronds and rhizomes of Drynaria sp. The figure shows six lines with different colors. The darker blue line represents “Drynaria quercifolia fertile fronds”. The red line represents “Drynaria rigidula fertile fronds”. The green line represents “Drynaria sparsisora fertile fronds”. The purple line represents “Drynaria quercifolia rhizome”. The lighter blue line represents “Drynaria rigidula rhizome”. The orange line represents “Drynaria sparsisora rhizome”

Full size image

As shown in Table 2, D. quercifolia fronds showed a high tyrosinase inhibition activity (exceeding 50 %) [32], and may therefore have possible commercial applications as a natural tyrosinase inhibitor, such as in the cosmetics industry (skin whitening) and food industry (antibrowning preservation) [5]. Interestingly however, most of the extracts exhibited tyrosinase enhancement activity, effectively acting as tanning agents. While reports on tyrosinase inhibition are more common, a number of extracts are known to increase melanogenesis, including kava rhizomes, lotus flowers and mangosteen leaves [33]. Although phenolic compounds are often tyrosinase inhibitors, several are capable of acting as tyrosinase activity enhancers, such as naringenin [5] and 4′-O-β-d-glucopyranosyl-(1→2)-β-d-glucopyranosyl-quercetin-3-O-β-d-glucopyranosyl-(1→4)-β-d-glucopyranoside [34]. Macrocycles such as cryptand and crown ethers are also capable of enhancing tyrosinase activity by acting as carriers for water molecules, which in turn increases the enzyme’s activity [35]. Tyrosinase enhancement can see application in skin care products designed to reduce UV damage for skin cancer prevention [34], and as a treatment for hypopigmentation [33]. It can also prove useful in the cosmetics industry, for self-tanning [33]. The exact causal agent for this tyrosinase enhancement would require further investigation, particularly in the fronds of D. sparsisora, which showed remarkable tyrosinase enhancement activity.

Table 2 Tyrosinase inhibition (%) of Drynaria sp fertile fronds and rhizomes (0.5 mg/mL)
Full size table

Conclusion

Of the three fern species screened, D. quercifolia fertile fronds exhibited the highest TPC, FRS, FRP and LPI. The fertile fronds of D. quercifolia and D. rigidula showed significantly higher TPC and FRP when compared to their rhizomes, with D. quercifolia fronds also exhibiting significantly higher FRS. D. sparsisora rhizomes on the other hand showed similar antioxidant activity with the fronds, with the exception of the rhizome’s FRS being significantly higher than that of the fronds. Interestingly, regardless of the differences in other antioxidant properties, the LPI between the fronds and rhizomes of all three species were comparable at the highest concentration studied. The fronds of D. quercifolia showed good tyrosinase inhibition, while the fronds of D. sparsisora showed remarkable tyrosinase enhancement. These findings may hopefully provide further impetus into looking at the fronds of other ferns which are commonly used mostly for their rhizomes.

References

  1. Lee JH, Park KH, Lee M, Kim H, Seo WD, Kim JY, Baek I, Jang DS, Ha TJ. Identification, characterisation, and quantification of phenolic compounds in the antioxidant activity-containing fraction from the seeds of Korean perilla (Perilla frutescens) cultivars. Food Chem. 2013;136(2):843–52.

    Article  CAS  PubMed  Google Scholar 

  2. Staszewski MV, Pilosof AMR, Jagus RJ. Antioxidant and antimicrobial performance of different argentinean green tea varieties as affected by whey proteins. Food Chem. 2011;125:186–92.

    Article  Google Scholar 

  3. Bansal S, Choudhary S, Sharma M, Kumar SS, Lohan S, Bhardwaj V, Syan N, Jyoti S. Tea: a native source of antimicrobial agents. Food Res Int. 2013;53(2):568–84.

    Article  CAS  Google Scholar 

  4. Cai Y, Luo Q, Sun M, Corke H. Antioxidant activity and phenolic compounds of 112 traditional Chinese medicinal plants associated with anticancer. Life Sci. 2004;74:2157–84.

    Article  CAS  PubMed  Google Scholar 

  5. Chang T. An updated review of tyrosinase inhibitors. Int J Mol Sci. 2009;10(6):2440–75.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  6. Higashi Y, Asanuma M, Miyazaki I, Ogawa N. Inhibition of tyrosinase reduces cell viability in catecholaminergic neuronal cells. J Neurochem. 2002;75(4):1771–4.

    Article  Google Scholar 

  7. Grimm J, Mueller A, Hefti F, Rosenthal A. Molecular basis for catecholaminergic neuron diversity. Proc Natl Acad Sci USA. 2004;101(38):13891–6.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Mithraja MJ, Irudayaraj V, Kiruba S, Jeeva S. Antibacterial efficacy of Drynaria quercifolia (L.) J. Smith (Polypodiaceae) against clinically isolated urinary tract pathogens. Asia-Pa. J Trop Biomed. 2012;2:S131–5.

    Article  Google Scholar 

  9. Chang HC, Agrawal DC, Kuo CL, Wen JL, Chen CC, Tsay HS. In vitro culture of Drynaria fortunei, a fern species source of Chinese medicine “Gu-Sui-Bu”. Vitro Cell Dev Biol Plant. 2007;43:133–9.

    Article  Google Scholar 

  10. Khan A, Haque E, Rahman MM, Mosaddik A, Rahman M, Sultana N. Isolation of antimicrobial constituent from rhizome of Drynaria quercifolia and its sub-acute toxicological studies. DARU. 2007;15(4):205–11.

    CAS  Google Scholar 

  11. Ramesh N, Viswanathan MB, Saraswathy A, Balakrishna K, Brindha P, Lakshmanaperumalsamy P. Phytochemical and antimicrobial studies on Drynaria quercifolia. Fitoterapia. 2001;72:934–6.

    Article  CAS  PubMed  Google Scholar 

  12. Sen A, Ghosh PD. A note on the ethnobotanical studies of some pteridophytes in Assam. Indian J Tradit Knowl. 2011;10:292–5.

    Google Scholar 

  13. Johnson T. CRC Ethnobotany Desk Reference. San Francisco: California CRC Press; 1999.

    Google Scholar 

  14. Yang F, Zhang C, Wu G, Liang S, Zhang X. Endangered Pteridophytes and their distribution in Hainan Island, China. Am Fern J. 2011;101(2):105–16.

    Article  Google Scholar 

  15. Wee YC. A Guide to the Ferns of Singapore. 3rd ed. Singapore: Singapore Science Centre; 2002.

    Google Scholar 

  16. Ranil RHG, Pushpakumara DKNG. Occurrence of Drynaria sparsisora (Desv.) T. Moore, in the lower Hantana area, Sri Lanka. J Natl Sci Found Sri Lanka. 2008;36(4):331–4.

    Google Scholar 

  17. Kähkönen MP, Hopia AI, Vuorela HJ, Rauha JP, Pihlaja K, Kujala TS, Heihonen M. Antioxidant activity of plant extracts containing phenolic compounds. J Agric Food Chem. 1999;47(10):3954–62.

    Article  PubMed  Google Scholar 

  18. Chang C, Yang M, Wen H, Chern J. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal. 2002;10(3):178–82.

    CAS  Google Scholar 

  19. Leong L, Shui G. An investigation of antioxidant capacity of fruits in Singapore markets. Food Chem. 2002;76(1):69–75.

    Article  CAS  Google Scholar 

  20. Miliauskas G, Venskutonis PR, van Beek TA. Screening of radical scavenging activity of some medicinal and aromatic plant extracts. Food Chem. 2004;85(2):231–7.

    Article  CAS  Google Scholar 

  21. Tan YP, Chan EWC. Antioxidant, antityrosinase and antibacterial properties of fresh and processed leaves of Anacardium occidentale and Piper betle. Food Biosci. 2014;6:17–23.

    Article  CAS  Google Scholar 

  22. Mau JL, Lai EYC, Wang NP, Chen CC, Chang CH, Chyau CC. Composition and antioxidant activity of the essential oil from Curcuma zedoaria. Food Chem. 2003;82(4):583–91.

    Article  CAS  Google Scholar 

  23. Singh N, Rajini PS. Free radical scavenging activity of an aqueous extract of potato peel. Food Chem. 2004;85:611–6.

    Article  CAS  Google Scholar 

  24. Kumazawa S, Taniguchi M, Suzuki Y, Shimura M, Kwon MS, Nakayama T. Antioxidant activity of polyphenols in carob pods. J Agric Food Chem. 2002;50:373–7.

    Article  CAS  PubMed  Google Scholar 

  25. Masuda T, Yamashita D, Takeda Y, Yonemori S. Screening for tyrosinase inhibitors among extracts of seashore plants and identification of potent inhibitors from Garcinia subelliptica. Biosci Biotech Biochem. 2005;69(1):197–201.

    Article  CAS  Google Scholar 

  26. Lim YY, Quah EPL. Antioxidant properties of Phyllanthus amarus extracts as affected by different methods. Food Chem. 2007;103:734–40.

    Article  CAS  Google Scholar 

  27. Lai HY, Lim YY. Evaluation of antioxidant activities of the methanolic extracts of selected ferns in Malaysia. Int J Environ Sci Dev. 2011;2:442–7.

    Article  Google Scholar 

  28. Chan EWC, Lim YY, Omar M. Antioxidant and antibacterial activity of leaves of Etlingera species (Zingiberaceae) in Peninsular Malaysia. Food Chem. 2007;104:1586–93.

    Article  CAS  Google Scholar 

  29. Elzaawely AA, Xuan TD, Tawata S. Essential oils, kava pyrones and phenolic compounds from leaves and rhizomes of Alpinia zerumbet (Pers.) B.L. Burtt. & R.M. Sm. and their antioxidant activity. Food Chem. 2006;103(2):486–94.

    Article  Google Scholar 

  30. Graβmann J. Terpenoids as plant antioxidants. Vitam Horm. 2005;72:505–35.

    Article  Google Scholar 

  31. Chandrasekara A, Shahidi F. Bioaccessibility and antioxidant potential of millet grain phenolics as affected by simulated in vitro digestion and microbial fermentation. J Funct Foods. 2012;4(1):226–37.

    Article  CAS  Google Scholar 

  32. Baurin N, Arnoult E, Scior T, Do QT, Bernard P. Preliminary screening of some tropical plants for anti-tyrosinase activity. J Ethnopharmacol. 2002;82:155–8.

    Article  CAS  PubMed  Google Scholar 

  33. Hamid MA, Sarmidi MR, Park CS. Mangosteen leaf extract increases melanogenesis in B16F1 melanoma cells by stimulating tyrosinase activity in vitro and by up-regulating tyrosinase gene expression. Int J Mol Med. 2012;29(2):209–17.

    PubMed  Google Scholar 

  34. Yamauchi K, Mitsunaga T, Batubara I. Novel quercetin glucosides from Helminthostachys zeylanica root and acceleratory activity of melanin biosynthesis. J Nat Med. 2013;67(2):369–74.

    Article  CAS  PubMed  Google Scholar 

  35. Broos J, Arends R, van Dijk GB, Verboom W, Engbersen JFJ, Reinhoudt DN. Enhancement of tyrosinase activity by macrocycles in the oxidation of p-cresol in organic solvents. J Chem Soc Perk T. 1996;1:1415–7.

    Article  Google Scholar 

Download references

Authors’ contributions

JTBL carried out all the laboratory bench work; collected and analyzed the data; and wrote this paper. LYY conceptualized the project design and provided advice and guidance throughout the project and writing of this paper. Both authors read and approved the final manuscript.

Acknowledgements

The authors wish to thank Monash University Malaysia for the financial support.

Compliance with ethical guidelines

Competing interests The authors declare that they have no competing interests.

Author information

Authors and Affiliations

  1. School of Science, Monash University Malaysia, Bandar Sunway, 46150, Petaling Jaya, Selangor, Malaysia

    Joash Ban Lee Tan & Yau Yan Lim

Authors
  1. Joash Ban Lee Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yau Yan Lim
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Joash Ban Lee Tan.

Rights and permissions

Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tan, J.B.L., Lim, Y.Y. Antioxidant and tyrosinase inhibition activity of the fertile fronds and rhizomes of three different Drynaria species. BMC Res Notes 8, 468 (2015). https://doi.org/10.1186/s13104-015-1414-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13104-015-1414-3

Keywords

  • Fern rhizome
  • Fertile fronds
  • Fern leaves
  • Free radical scavenging
  • Tyrosinase inhibition

BMC Research Notes

ISSN: 1756-0500

Contact us