Indian Journal of Natural Products and Resources, Vol. 4(4), December 2013, pp. 363-370

Evaluation of phytochemical, antioxidant and antimicrobial activities of L. species from Western Ghats

A R Sivu1, #, N S Pradeep1*, K B Rameshkumar2 and A G Pandurangan1 1Plant Systematic and Evolutionary Science Division, 2Phytochemistry and Phytopharmacology Division Jawaharlal Nehru Tropical Botanic Garden and Research Institute, Palode, Thiruvananthapuram-695 562, Kerala, India

Received 18 April 2012; Accepted 29 July 2013

The genus Memecylon L. is a least explored group of and the present study reports the preliminary phytochemical and pharmacological evaluation of 32 Memecylon species collected from the Western Ghats. Among these 4 are rare and endangered and 16 endemic. The methanolic extracts of the were evaluated for their phenolic and flavonoid contents, in vitro antioxidant and antimicrobial activities. Phenolic contents of the methanol extracts of leaves were comparatively low in the species, ranging from 89.86 mg/g (M. gracile Bedd.) to 05.04 mg/g (M. depressum Benth.). Flavonoid compounds were highest in M. grande Retz. (39.56 mg/g) and lowest in M. talboltianum Brandis (07.60 mg/g). The in vitro free radical scavenging assay was done using DPPH method and the results showed moderate activities to the extracts. The highest antioxidant activity was observed for M. heyneanum Benth. (IC50=15.30 µg/mL). Antibacterial activity against three Gram- positive and six Gram- negative bacteria was tested by disc diffusion method and the leaf extracts showed remarkable broad spectrum antibacterial activity, especially for M. deccanense Clarke, M. terminale Dalzell, M. heyneanum Benth., M. clarkeanum Cogn. and M. sessile Benth.

Keywords: Memecylon species, Western Ghats, Phenolics, Flavonoids, Antioxidant, Antibacterial. IPC code; Int. cl. (2011.01)−A61K 36/00.

Introduction The genus Memecylon L. is among the least explored India has a rich floristic diversity with 46, 550 group of plants and hence an attempt has been made species that accounts for about 11% of the total to evaluate their phytochemical and pharmacological world flora, of which 28 % are endemic to the potential. 1 country . Among the four hot spots of floristic The genus Memecylon L., belonging to the diversity in India, the Western Ghats hosts nearly family , is represented world over 4500 flowering plants are endowed with high by around 250 species of shrubs and trees in the endemism with nearly 1500 endemics. Most of paleotropical region3. They are distributed in all the floristic wealth, especially the endemic species types of habitats ranging from deciduous, semi remains unexplored regarding their potential utility evergreen, evergreen and montane forests with a wide and the chemical constituents or bioactivities. range of altitude from sea level to 2000 m. In India The wild underutilised plants have become an the genus Memecylon is represented by 39 species of interesting source of nutraceutical, healthcare, which 21 are endemic to the country and the Western cosmetic and food industries. Indiscriminate Ghats is reported to host 29 species4-8. However, exploitation, habitat destruction and introduction while studying the molecular of the genus of exotic species lead to the reduction of population Memecylon L. of the Western Ghats, the authors did of the endemic, rare and endangered species and collect 3 more Memecylon species (M. procerum Thw., therefore there is an urgent need to conserve these M. clarkeanum Cogn. and M. parvifolium Thw.) as species along with evaluation of their potentialities. new records to India (Plate 1). Among 32 species —————— collected from the Western Ghats, 4 species, viz. *Correspondent author: M. lawsonii Gamble, M. lushingtonii Gamble, Phone: 0472 2869226 E-mail: [email protected] M. flavescens Gamble and M. sisparense Gamble # Present Address: Department of Botany, NSS College Nilamel, comes under rare and endangered categories (Plate 1), 9 Kollam-691 535, Kerala while 16 species are endemic to the region (Table 1). 364 INDIAN J NAT PROD RESOUR, DECEMBER 2013

Plate 1—Common Memecylon species (a: M. umbellatum, b: M. edule and c: M. randerianum); Rare and endangered species (d: M. sisparense, e: M. lawsonii, f: M. flavascence and g: M. lushingtonii); New records to India (h: M. parvifolium, i: M. procerum and j: M. clarkeanum)

SIVU et al.: PHYTOCHEMICAL, ANTIOXIDANT AND ANTIMICROBIAL ACTIVITIES OF MEMECYLON L. SPECIES 365

Memecylon species are utilized world wide as (locally known as Kasavu, Kayampoo, Kanalei). The timbers, ornamentals, source of edible fruits and plant is popular as ornamental tree and widely used in yellow dye in addition to their medicinal properties3. traditional medicines and also as source of food, dye Among the different Memecylon species, M. umbellatum and timber. The pulpy, astringent ripe of the Burm., is the most common species (Plate 1), distributed tree are edible and are eaten in time of famine. in India and Sri Lanka and known as ‘iron wood tree’ The leaves yield a yellow dye and in combination

Table 1—Total phenolic, flavonoid compounds and DPPH scavenging activity of the leaf methanol extracts of Memecylon species

M. sp. Memecylon species Voucher Total Total IC50 values ID No Phenolics Flavonoids (µg/mL) M 1 M. agastyamalaianum Santhosh et al * 65102 38.03 ± 0.02 08.40 ± 0.04 87.01 ± 0.01 M 2 M. angustifolium Wight 65106 23.97 ± 0.02 10.03 ± 0.04 87.08 ± 0.02 M 3 M. capitellatum L. 63524 06.04 ± 0.02 31.93 ± 0.04 115.37 ± 0.04 M 4 M. depressum Benth. * 61748 05.04 ± 0.01 17.76 ± 0.03 128.13 ± 0.03 M 5 M. flavescens Gamble* 65126 05.05 ± 0.01 11.23 ± 0.04 115.17 ± 0.04 M 6 M. gracile Bedd. * 65104 89.86 ± 0.04 08.42 ± 0.01 58.56 ± 0.04 M 7 M. grande Retz. 61736 09.90 ± 0.04 39.56 ± 0.04 64.00 ± 0.02 M 8 M. heyneanum Benth. 63543 61.06 ± 0.03 12.40 ± 0.04 15.30 ± 0.03 M 9 M. clarkeanum Cogn. 63600 59.96 ± 0.04 11.30 ± 0.03 97.37 ± 0.01 M 10 M. lushingtonii Gamble 65146 10.13 ± 0.03 16.70 ± 0.03 148.23 ± 0.04 M 11 M. malabaricum (C. B. Clarke.) Cogn. 63518 25.76 ± 0.03 12.56 ± 0.05 207.24 ± 0.03 M 12 M. rivulare Bremer 61767 15.83 ± 0.04 13.63 ± 0.03 141.20 ± 0.02 M 13 M. sessile Benth. 65120 82.83 ± 0.03 09.16 ± 0.04 40.10 ± 0.04 M 14 M. sisparense Gamble* 65124 30.36 ± 0.06 09.13 ± 0.04 44.06 ± 0.02 M 15 M. sivadasanii Mohanan et al * 61775 14.06 ± 0.01 10.80 ± 0.02 55.10 ± 0.03 M 16 M. subramanii Henry* 63564 09.46 ± 0.04 14.96 ± 0.04 91.06 ± 0.03 M 17 M. talboltianum Brandis* 65161 11.03 ± 0.05 07.60 ± 0.03 114.0 ± 0.02 M 18 M. terminale Dalzell* 65162 65.96 ± 0.15 10.60 ± 0.02 232.47 ± 0.03 M 19 M. umbellatum Burm. 61751 10.10 ± 0.03 15.33 ± 0.05 62.43 ± 0.04 M 20 M. wightii Thw. 63584 06.78 ± 0.03 09.56 ± 0.04 77.21 ± 0.02 M 21 M. mundanthuraianum Viswanathan & Manik.* 65116 51.76 ± 0.04 07.53 ± 0.03 214.27 ± 0.05 M 22 M. bremeri Viswanathan 65136 10.75 ± 0.03 20.33 ± 0.04 53.90 ± 0.03 M 23 M. manickamii Murugan et al * 65171 14.10 ± 0.03 12.50 ± 0.04 85.37 ± 0.03 M 24 M. courtalensis Manickam et al * 63540 05.63 ± 0.05 09.00 ± 0.02 74.22 ± 0.02 M 25 M. tirunelvelicum Murugan et al * 65121 23.73 ± 0.05 13.53 ± 0.04 149.97 ± 0.04 M 26 M. royenii Blume 65138 07.83 ± 0.03 12.50 ± 0.04 145.17 ± 0.04 M 27 M. deccanense Clarke* 65165 67.06 ± 0.01 08.46 ± 0.04 110.00 ± 0.05 M 28 M. edule Roxb. 63558 08.73 ± 0.04 14.36 ± 0.03 82.43 ± 0.03 M 29 M. parvifolium Thw. 63563 64.10 ± 0.03 10.40 ± 0.05 162.37 ± 0.05 M 30 M. procerum Thw. 61752 05.90 ± 0.10 18.20 ± 0.03 103.97 ± 0.03 M 31 M. lawsonii Gamble* 61761 08.83 ± 0.03 12.43 ± 0.04 114.17 ± 0.02 M 32 M. sylvaticum Thw. 61726 15.86 ± 0.02 15.30 ± 0.05 78.13 ± 0.02 * Endemic to the Western Ghats. Phenolic contents: mg gallic acid equivalent per g dry weight of leaves methanol extract. Flavonoid contents: mg quercetin equivalent per g dry weight of leaves methanol extract. Values are mean ± SD of triplicate experiments.

366 INDIAN J NAT PROD RESOUR, DECEMBER 2013

with myrobalans and sappan wood it produces oleanolic acid, ursolic acid, sitosterol-β-D-glucoside bright red tinge10. In traditional medicines, leaves of and umbelactone have been isolated from the aerial M. umbellatum has been used as a cooling astringent, parts of M. umbellatum Burm.35. The roots yielded, in conjunctivitis as a lotion and given internally in octocosonoic acid, cerotic acid, ethyl palmitate, leucorrhoea and gonorrhoea11. The leaves are also palmitic acid and butyric acid36. used for the treatment of diabetes12, in the treatment The present study reports the quantitative estimation of bone fracture13, herpes14, skin diseases15 and snake of the phenolic compounds and flavonoids of the bite16. The leaves and barks are applied to bruises10. methanol extracts of the leaves of 32 Memecylon The decoction of the root is used in excessive species distributed in the Western Ghats region of menstrual discharge17,18. The seeds are used to cure India along with their in vitro free radical scavenging cough and are sedative19. Biological activities like activities and antimicrobial activities. anti-diabetic20-21, antibacterial22, antiviral23 and wound 24 Materials and Methods healing activities of M. umbellatum leaves have 25 been reported. The roots also possess analgesic and Plant Material hepatoprotective26 activities. Fresh leaves of the Memecylon species (Table 1) Roxb. is another common were collected from different localities, including type species (Plate 1), well known for its use as a mordant localities in the Western Ghats region and voucher in silk dyeing. Treatment with the leaf of M. edule is herbarium specimens were deposited in Jawaharlal said to heal burning wounds without any scar. The Nehru Tropical Botanic Garden and Research anti-inflammatory, analgesic and antioxidant activities Institute Herbarium (TBGT). of the leaves supported the traditional use of the Extraction 27 leaves in relieving inflammation and pain . The dry leaf powder of the 32 Memecylon species Decoction of roots and heartwood has also been used (10 g each) were extracted with methanol using a to relief fever symptoms of several diseases such as Soxhlet apparatus for 4 h. The vacuum dried extracts 27 common cold, measles and chicken-pox . The were stored at 4o C until further analysis. antibacterial activity of the seed extract of M. edule has also been evaluated28. M. malabaricum Cogn. Estimation of total phenolic compounds (syn. M. randerianum Almeida & Almeida). Modified Folin-Ciocalteu reagent colorimetric method was used for the determination of total is a common species (Plate 1) and decoction 37 of the flowers and twigs is used to treat skin diseases phenolics . The methanol extract (0.5 mL) was and chicken pox10. A paste of young shoot tips mixed with 5 mL Folin- Ciocalteu reagent (1:10 and cumin seeds are applied against herpes and dilution with distilled water). After 5 min, 4 mL of the decoction of young leaves in combination is 20 % sodium carbonate solution was added. The taken against stomach disorders29. The leaves possess mixture was allowed to stand for 15 minutes and the antimicrobial activity30-31. The leaves of M. lushingtonii absorbance was measured at 765 nm. Total phenolics Gamble has been reported as an effective post-coital were estimated as gallic acid equivalent (GAE) mg/g contraceptive32. The bark of M. angustifolium Wight is dry weight of the extract from the calibration curve used as a tonic and refrigerant18. using standard gallic acid (10 -50 µg) in methanol.

Out of the 32 Memecylon species collected from Estimation of total flavonoids the Western Ghats region, literature survey shows that Aluminium chloride colorimetric method was used only M. umbellatum has been studied for their for total flavonoids determination38. Methanol extract chemical constituents. Preliminary phytochemical (0.5 mL) was mixed with 1.5 mL of methanol, 0.1 mL screening revealed the presence of phenolic of 10 % aluminum chloride, 0.1 mL of 1 M potassium compounds, flavonoids, steroids and terpenoids in acetate, 2.8 mL of distilled water and left at room different extracts of the leaves of M. umbellatum22. temperature for 30 minutes. Absorbance of the The proximate components, nutritive values and reaction mixture was measured at 415 nm. Total elemental analysis of the leaves have been reported33. flavonoids were estimated from the calibration curve Tannins have been reported in significant quantity using standard quercetin (10-50 µg) in methanol and in the bark, followed by leaves, roots, stem and the results are expressed as quercetin equivalent mg/g of M. umbellatum34. α-Amyrin, sitosterol, dry weight of extract. SIVU et al.: PHYTOCHEMICAL, ANTIOXIDANT AND ANTIMICROBIAL ACTIVITIES OF MEMECYLON L. SPECIES 367

DPPH radical scavenging assay determination of total phenolic content of plants due Radical scavenging activity was determined by to its high sensitivity and reproducibility. All the spectrophotometric method based on the reduction of Memecylon species studied contained phenolics the stable free radical 2, 2-diphenyl- 1-picrylhydrazyl and are distributed in differential quantities. The 39 (DPPH) . Diluted methanol extracts were added at total phenolic content varied from 05.04 mg/g an equal volume to a methanolic solution of DPPH (M. depressum Benth.) to 89.86 mg/g (M. gracile (200 µM DPPH). After 15 min. at room temperature, Bedd.). Total phenolic content was greater than the absorbance was recorded at 517 nm. The activity 50 mg/g extract for M. gracile (89.86 mg/g), was measured as percentage, calculated using the M. sessile Benth. (82.83 mg/g), M. deccanense formula: Clarke (67.06 mg/g), M. terminale Dalzell

% scavenging = [(Acontrol-Asample)/Acontrol] x 100. (65.96 mg/g), M. parvifolium Thw. (64.10 mg/g), M. heyneanum Benth. (61.06 mg/g), M. lawsonii The activity was reported as IC value; the 50 Gamble (59.96 mg/g) and M. mundanthuraianum concentration of sample (µg/mL) required to scavenge Viswanathan & Manik (51.76 mg/g). 50 % of DPPH radical, relative to the control (DPPH Total flavonoid content was measured without antioxidant agents added). Ascorbic acid was spectrophotometrically based on aluminium chloride used as positive control. complex formation. The flavonoid concentration in Antibacterial assay the methanol extracts of the dried leaves of Antibacterial activities of the extracts were Memecylon species in terms of mg quercetin screened by the disc diffusion assay40 and the equivalent (QE) per g leaf methanol extract are activities were reported as diameter of the inhibition presented in Table 1. The highest content of zones that includes the disc diameter (6 mm) also. flavonoids was found in M. grande Retz. (39.56), The concentrated methanol extracts were redissolved followed by M. capitellatum L. (31.93) and in DMSO and 10 µL of the DMSO extracts M. bremeri (20.33). The lowest flavonoid content was (10 mg/mL) were spotted on Whatman No. 1 filter found in M. talboltianum Brandis (07.60 mg/g). paper discs of 6 mm diam. and aseptically applied to Antioxidant activity of the extracts the surface of agar plates at well-spaced intervals. The DPPH method is a simple, rapid and sensitive Authentic strains of Gram-positive [Bacillus subtilis method accepted widely for screening of samples (MTCC 741), B. cereus (MTCC 430), Staphylococcus for radical scavenging activity41. Table 1 shows aureus (MTCC 96)] and Gram-negative [Klebseilla the quantity of each extract needed for 50% pneumonia (MTCC 109), Pseudomonas aeruginosa scavenging of the DPPH free radical (IC50). IC50 (MTCC 741), Escherichia coli (MTCC 443), Proteus of the standard compound quercetin was found to vulgaris (MTCC 426), Serratia marcescens (MTCC be 10.16 (±1.75) µg/mL. The highest radical 97), Salmonella typhii (MTCC 733)] bacteria obtained scavenging activity was shown by M. heyneanum from Microbial Type Culture Collection (MTCC), Benth. (IC 15.30 µg/mL), followed by M. sessile maintained at the Institute of Microbial Technology, 50 Benth. (IC 40.10 µg/mL) and M. sisparense Gamble Chandigarh, India were used for the assays. Control 50 discs impregnated with 10 µL of the solvent DMSO (IC50 44.06 µg/mL), while the activity was least for and the standard drug streptomycin (2 µg per disc) M. terminale Dalzell (IC50 232.47 µg/mL). were used alongside the test discs in each experiment. Of the different class of secondary metabolites, phenolic compounds and particularly flavonoids are Statistical analysis important considering their effects on human nutrition The experiments were replicated thrice and the and health are considerable. The beneficial effects of phenolic compounds have been attributed mainly results are expressed as mean ±SD. 42 to their antioxidant activity . Free radicals are Results and Discussion involved in many disorders like neurodegenerative diseases, cancer and AIDS. Antioxidants through their Phenolic and flavonoid contents scavenging activities are useful for the management The total phenolic content expressed as mg of those diseases. Currently available synthetic GAE/g of the Memecylon species are presented in antioxidants are causing serious side effects and Table 1. The method provides a simple test for secondary metabolites from plants are emerging as 368 INDIAN J NAT PROD RESOUR, DECEMBER 2013

promising substitutes for the synthetic ones. The moderate to good activity against the tested bacterial search for natural antioxidants of dietary, cosmetic strains, especially for M. deccanense, M. terminale, and pharmaceutical potential has become a major M. heyneanum, M. clarkeanum and M. sessile. industrial and scientific pursuit recently. The highest inhibition zone (26 mm) was shown by M. agastyamalaianum Santhosh et al against Bacillus Antibacterial activity subtilis and Proteus vulgaris, M. heyneanum and The antibacterial activity of different species of M. deccanense Clarke against Proteus vulgaris Memecylon extracts were tested against a group of and M. parvifolium against Escherichia coli. clinically important bacterial strains by disc diffusion M. deccanense showed remarkable activity against all assay and the results are reported in Table 2 as the tested organisms, with greater zone of inhibition zone of inhibition (mm). The results revealed than the standard drug at the tested concentrations,

Table 2—Antibacterial activity of methanol extracts of leaves of Memecylon species [Zone of inhibition (mm) by disc diffusion assay]

M. sp ID* B. c S. a B. s E. c K. p P. a P. v S. t S. m M 1 9 9 26 9 18 13 26 21 12 M 2 12 9 24 11 18 9 14 9 9 M 3 11 8 12 8 16 9 13 11 10 M 4 12 10 14 9 16 14 11 8 8 M 5 10 8 14 10 10 9 11 9 NA M 6 16 9 21 14 24 17 18 18 11 M 7 20 11 11 9 9 10 10 9 9 M 8 22 15 21 13 16 11 20 19 10 M 9 19 18 18 14 16 14 26 18 20 M 10 10 9 11 8 9 11 9 9 11 M 11 10 10 10 8 14 12 9 9 9 M 12 9 9 9 8 10 12 10 9 17 M 13 18 18 16 18 18 20 18 11 10 M 14 10 9 12 10 14 14 22 10 9 M 15 10 11 21 10 12 11 14 8 8 M 16 9 9 14 NA 16 11 22 9 10 M 17 10 10 11 21 14 13 11 9 10 M 18 21 20 20 19 24 21 20 17 18 M 19 11 9 14 9 16 9 9 10 9 M 20 10 9 12 10 10 11 10 9 8 M 21 10 10 10 9 11 12 13 9 11 M 22 9 9 12 9 11 12 16 9 23 M 23 12 9 13 9 12 13 12 9 9 M 24 9 11 16 16 11 16 20 8 13 M 25 10 9 11 9 14 11 14 9 10 M 26 9 8 13 10 9 10 11 9 6 M 27 21 22 24 24 24 24 26 24 23 M 28 11 9 10 11 12 9 11 8 11 M 29 9 9 20 26 18 21 20 12 12 M 30 16 10 24 10 9 11 18 8 11 M 31 11 14 16 12 10 13 14 8 11 M 32 10 11 11 NA 10 11 NA 11 7 Std 17 22 21 10 16 15 20 16 17 * Leaves methanol extracts of Memecylon species 100 µg/disc (see Table 1 for species name). B. s: Bacillus subtilis; B. c: Bacillus cereus and S. a: Staphylococcus aureus (Gram-positive bacteria) and K. p: Klebseilla pneumonia, P. a: Pseudomonas aeruginosa, E. c: Escherichia coli, P. v: Proteus vulgaris, S. m: Serratia marcescens, S. t: Salmonella typhii (Gram-negative bacteria). Zone of inhibition in mm; Std: Standard antibacterial compound streptomycin (2µg/disc). NA: No activity. SIVU et al.: PHYTOCHEMICAL, ANTIOXIDANT AND ANTIMICROBIAL ACTIVITIES OF MEMECYLON L. SPECIES 369

while M. terminale showed greater zone of inhibition endangered and endemic species, showed remarkable than the standard drug against all except antibacterial activity and presence of phenolic and Staphylococcus aureus, Bacillus subtilis and Proteus flavonoid compounds and moderate to good free vulgaris. M. sylvaticum Thw. and M. flavascence radical scavenging activities, suggesting elaborate Gamble showed no inhibition against Escherichia coli, investigation of the genus for isolation and Proteus vulgaris and Salmonella marascens. All characterisation of constituents and evaluation of the other samples showed inhibition in the range biological activities. Present study also highlights the 7-25 mm against all the tested organisms. The present potential of the extensive floristic wealth of the investigation revealed remarkable antibacterial Western Ghats region yet to be exploited. activities of the Memecylon species against the tested bacterial strains. The screening of plants for Acknowledgements antimicrobial activity assumes particular significance The authors thank the Director, JNTBGRI for in the context of recent emergence of infectious providing facilities, Dr. E. S. Santhosh Kumar, diseases and an increased resistance of some JNTBGRI for identification of the plant materials. pathogenic microorganisms to the existing drugs. Among the Memecylon species studied, the most References common are M. umbellatum Burm., M. malabaricum 1 Plant Discoveries 2010, Botanical Survey of India, Kolkata, (syn. M. randerianum) and M. edule Roxb. 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