1. INTRODUCTION:

Pteridophytes, a Ferns and Ferns allies plant group, have been widely used as a source of medicine and possess diverse biological activities. Pteridophytes are a vital component of traditional medicine in many countries for the treatment of fever, skin diseases, ulcers, and stomach ache¹. There is growing interest in phytochemicals hailed as "a gift from plants to humans," as they have various health benefits². Therefore, it is of utmost importance to screen pteriodophyte diversity for medically beneficial compounds for treating human and plant diseases. In recent years, the search for phytochemicals with antioxidant, antimicrobial, and anti-inflammatory properties has increased owing to their potential use in treating various chronic and infectious diseases³.

Studies have also reported the antiviral, antifungal and antimicrobial activity of some Pteridophytes^4,5,6,7. In addition to their bioactivity, many pteridophytes possess antioxidant activities⁸. Antioxidants are known to curb the activities of free radicals and other reactive oxygen species and pathogenic agents involved in diseases such as asthma, inflammatory arthropathies, diabetes, and other diseases. Reactive oxygen species are also responsible for aging^9,10. Although there are many reports on the folklore medicinal uses of pteridophytes, studies on the pharmacology of phytochemicals have mainly focused on higher plant groups rather than pteridophytes, as they exhibit greater biodiversity, more varied adaptations, and are more widely distributed, making them accessible to a significant number of research groups¹¹. However, with advancements in science, the desire to tap for new resources has led to studies of certain pteridophytes and their secondary metabolites. Knowing the potential aspects of pteridophytes as many candidates among plants with medicinal properties, the present study focuses on the profiling of L. cernua L. (Figure 1), a lesser-known and traditionally used pteridophyte by the very few tribes in Mizoram. Although L. cernua is a widely distributed species recognized for several uses in traditional medicine in other countries, reports are available to validate its medicinal potential. The present study provides insight into the first report on the bioactivity of L. cernua from the region and India. However, the data obtained from this study represent only a small part of what needs to be discovered for this spe

Figure 1: L.cernua in its natural habitat

2. MATERIALS AND METHODS:

2.1. Collection and Identification of Plants:

L.cernua (L.) Pic. Serm. was collected from Murlen National Park, Mizoram, and the field data were recorded. The specimens collected were identified based on their morphological characteristics and were compared with voucher specimens from the National Botanical Research Institute (NBRI), Lucknow and Botanical Survey of India (BSI), Shillong. The specimen is presented under families according to the classification system proposed by Pichi-Sermolli¹² and the added literature^13,14. Pichi Sermolli¹⁵ has been followed for the correct citation of the species author. The collected specimens were deposited in the Herbarium Collection, Department of Botany, Mizoram University, for future reference.

2.2. Preparation of Plant Extracts:

The dried aerial parts of L. cernua (L.) Pic. Serm. was pulverized to powder form and subjected to sequential continuous hot extraction in a Soxhlet apparatus using chloroform and methanol as the solvents. The extraction was performed for 72 h. The extracts were concentrated using a vacuum rotary evaporator (Buchi Rotavapor® R-215). The plant extracts produced in the semi-solid mass were refrigerated at 4°C until further use. Henceforth, chloroform and methanol extracts of L. cernua are known as LCCE (L. Cernua Chloroform Extract) and LCME (L. Cernua Methanol Extract), respectively.

2.3. Qualitative Phytochemical Analysis:

The following methods and tests for alkaloids, carbohydrates, proteins, tannins, terpenoids, phenols, glycosides, saponins, phytosterols, and saponins described by Kokate et al.¹⁶ were used for the screening of phytochemicals.

2.4 Antibacterial Test:

Antimicrobial susceptibility was tested on solid media in Petri plates using the agar well diffusion method^17,18. The test was conducted on two gram-negative bacteria, namely Escherichia coli (ATCC - 10536) and Klebsiella pneumoniae (ATCC - 10031), and a gram-positive bacterium, Bacillus subtilis (ATCC- 11774). Plant extracts were prepared at different concentrations (20, 40, 60, and 80mg ml^-1 using the serial dilution method. 70.0µL of different concentrations of plant extracts were added to the wells using a sterile syringe and allowed to diffuse at room temperature. Negative control plates containing inocula without plant extracts were used. The known broad-range antibiotic ceftriaxone was used as a positive control. The plates were incubated at 37°C for 18–24h. The diameter of the inhibition zone (mm) was measured and the activity index was calculated. Triplicates were maintained, and the experiment was repeated three times. The readings were taken in three different fixed directions for each replicate, and the average values were recorded.

2.5 Determination of Total Phenolic Content:

The total phenolic content of LCCE and LCME was determined using the method described by McDonald et al.¹⁹, with slight modifications. Gallic acid was used as the standard to prepare a calibration curve. Using a calibration curve, the phenolic content of the extracts was determined and expressed as milligrams of Gallic acid equivalent (GAE) per gram of dried plant material. The experiment was repeated thrice.

2.6 Determination of Total Flavonoid Content:

The total flavonoid content of the extracts was determined using the aluminium chloride method with Quercetin as a standard²⁰. The total flavonoid content of the extracts was determined and expressed as milligrams of Quercetin equivalents (mg QE) per gram of extract. The experiment was repeated three times, and the values were expressed.

2.7 Determination of Antioxidant Capacity:

DPPH (2, 2-diphenyl-1-picrylhydrazil) free radical scavenging assay was performed according to the method described by Kim et al^.21. Standard stock solutions of LCCE and LCME were prepared by dissolving 10.0mg of the plant extract in 10.0ml of distilled water. Solutions of 0.0005, 0.001, 0.005, 0.01, 0.025 and 0.05mg ml^-1 solutions of each extract were prepared from the stock solution. Absorbance was measured at 517nm using a Thermo Scientific EVOLUTION 200UV-visible spectrophotometer. The percentage of inhibition was calculated by comparing the absorbance values of the test samples with those of the control samples (not treated with the extract). Inhibition percentage (I) was calculated as follows:

Control absorbance – Sample absorbance

I(%) = ------------------------------------------------- X 100

Control absorbance

3. RESULTS:

The results of the phytochemical tests of LCCE and LCME are presented in Table 1. The results revealed the presence of alkaloids, carbohydrates, proteins, tannins, terpenoids, phenols, glycosides, saponins, phytosterols, and flavonoids. However, LCCE showed the most significant phytochemical diversity.

Table 1: Qualitative phytochemical analysis of LCCE and LCME.

Phytochemical compounds	LCCE	LCME
Alkaloids	-	+
Carbohydrates	+	-
Proteins	+	-
Tannins	+	-
Terpenoids	+	-
Phenols	+	+
Glycosides	+	+
Saponins	+	-
Phytosterols	+	+
Flavanoids	+	+

+ = present; - = absent

3.1. Antibacterial activity of L. cernua (L.) Pic. Serm. extract against Escherichia coli, Klebsiella pneumoniae and Bacillus subtili:

The antibacterial activities of LCCE and LCME were examined using the agar well diffusion method. The assessment of antibacterial activity was based on the determination of the diameter of the zone of inhibition (mm) formed around the well filled with the extract.

The 20, 40, 60 and 80mg ml^-1of LCME caused 7.00±0.0, 7.5±0.0, 7.83±0.29 and 14.33±0.57mm inhibition zone in the agar plate of E. coli, respectively (Figure 2). The positive control on the other hand, produced an inhibition zone of 25mm. The antimicrobial proficiency of 80mg ml^-1 LCME against E. coli was 57.3% compared with the positive control. Therefore, it is suggested that LCME at 80mg ml^-1 was the most potent in inhibiting E. coli.

The 20, 40, 60 and 80mg ml^-1 of LCME caused 7.83±0.23, 9.2±0.57, 10.33±0.67 and 12.00±0.57mm inhibition zone in the agar plate of K. pneumoniae, respectively (Figure 3). The positive control caused an inhibition zone of 24.0±0.00mm. The inhibitory potential of LCME increased with an increase in the extract concentration. The antimicrobial efficiency of 80 mg ml^-1 of LCME against K. pneumoniae was 50% compared to that of the positive control.

The 20, 40, 60 and 80mg ml^-1of LCME caused 7.0±0.00, 7.5±0.03, 8.0±0.00 and 9.0±0.00mm inhibition zone in the agar plate of B. subtilis, respectively (Figure 4). The positive control resulted in a zone of inhibition of 22 mm. The antimicrobial efficiency of 80mg ml-1 of LCME against B. subtilis was 41% compared to that of the positive control.

Figure 2: The antibacterial activity in the methanolic extract of L. cernua (L.) Pic. Serm. against E. coli. The values are mean of three replicates. Vertical bars show ±SE.

Figure 3: The antibacterial activity in the methanolic extract of L.cernua (L.) Pic. Serm. against Klebsiella pneumoniae. The values are mean of three replicates. Vertical bars show ±SE.

Figure 4: The antibacterial activity in the methanolic extract of L. cernua (L.) Pic. Serm. against Bacillus subtilis. The values are mean of three replicates. Vertical bars show ±SE.

These results suggest that LCME has the most potent antibacterial activity against E. coli, followed by K. pneumoniae and B. subtilis. The results also indicated that gram (-) bacteria were more sensitive to LCME.

3.2 Total Polyphenol Content and Total Flavonoids Content:

The Total Phenolic Content and Total Flavonoid Content in LCCE and LCME were determined from the calibration curve (Figure 5 and Figure 6) and results are shown in Table 2.

Figure 5: Calibration curve for gallic acid

Figure 6: Calibration curve for quercetin.

Table 2: Total Phenol content in mg GAE/g and Flavonoid Content in mg QE/g of LCCE and LCME. Values are mean of three replicates ± SD.

Extract	Total phenol	Total flavonoid
LCCE	134.60±0.03	116.90±0.02
LCME	137.50±0.01	131.60±0.02

The phenolic content in LCME was 137.5mg GAE g^-1 and that of LCCE was found to be 134.0mg GAE g^-1. However, flavonoid content in LCME was 131.6 mg QE g^-1 which was comparatively higher than that of LCCE which was 116.90mg QE g^-1. These results suggest that solvent selection for extraction profoundly affects the yield and quantification of flavonoids in plants.

3.3. DPPH RADICAL SCAVENGING ACTIVITY AND IC₅₀

The antioxidant activity of LCCE and LCME was determined using a methanolic solution of DPPH reagent.

Table 3. Results of DPPH radical scavenging assay of BHT. Values are mean ± SD of three replicates.

Extract	Concentration (µg ml^-1)	DPPH Scavenging activity, I (%)	IC₅₀ (µg ml^-1)
BHT	10.0	52.73±0.001	2.62
	20.0	55.38±0.001
	40.0	65.20±0.002
	60.0	72.10±0.001
	80.0	81.05±0.003
	100.0	85.35±0.003

Table 4: Results of DPPH radical scavenging assay of LCCE. Values are mean ± SD of three replicates.

Extract	Concentration (µg ml^-1)	DPPH Scavenging activity, I (%)	IC₅₀ (µg ml^-1)
LCCE	10.0	45.38±0.001	39.07
	20.0	47.69±0.007
	40.0	50.0±0.001
	60.0	53.07±0.00
	80.0	56.15±0.003
	100.0	59.23±0.003

Table 5. Results of DPPH radical scavenging assay of LCME. Values are mean ± SD of three replicates.

Extract	Concentration (µg ml^-1)	DPPH Scavenging activity, I (%)	IC₅₀ (µg ml^-1)
LCME	10.0	52±0.004	15.44
	20.0	54.4±0.004
	40.0	55.2±0.004
	60.0	63.2±0.004
	80.0	68.0±0.004
	100.0	72.8±0.004

The antioxidant activities of BHT (Table 3), LCCE (Table 4) and LCME (Table 5) are expressed in terms of the percentage of DPPH scavenging activity and IC50 values in μg ml^-1. BHT (Butylated hydroxytoluene) was used as the standard compound, parallel to the examination of the antioxidant activity of plant extracts; the values for the standard compound were obtained and compared to the values of the plant extract.

The DPPH scavenging assay showed that LCME had 7.2-fold higher antioxidant activity than LCCE, as indicated by the IC50 values obtained for both extracts. These results suggested that the methanolic extract had better antioxidant activity than the chloroform extract.

4. DISCUSSION:

In the present study, phytochemical screening of LCCE showed the presence of carbohydrates, proteins, terpenoids, phenols, glycosides, saponins, phytosterols, and flavonoids, whereas alkaloids and tannins were absent. In the methanol extract, all phytochemicals tested were present in addition to carbohydrates, tannins, and terpenoids. In comparison, the study on L. cernua in the Philippines by Porquis et al.²², showed only two phytochemicals (saponins and terpenoids) out of seven tests performed on both aerial and ground parts. Also, Choung et al.²³confirm the presence of alkaloids in L. cernua, which shows a difference in their phytoconstituents when compared with the study made by Porquis et al.²². The diverse phytoconstituents in both plants may be because of the environmental influence in a species²⁴. Therefore, it is necessary to refer to the report of Liu et al.²⁵, who found that climatic and edaphic factors greatly influence the production of active substances in plants like Sinopodophyllum hexandrum (Royle) T.S. Ying and places like Jingyuan, Ningxia Province, Yongdeng and Gansu Province flavored the production of podophyllotoxin and lignans in S.hexandrum, but in Shangri-La, Yunnan Province, and Nyingchi, Tibet the conditions were favorable for quercetin and kaempferol production in the same species²⁵. In addition, solvent selection may profoundly also influence the phytochemical profile of plants.

In the present study, we further evaluated the methanolic extract of L. cernua. for antibacterial activity, because it demonstrated an intermediate diversity of phytochemicals in comparison to the chloroform extract. The remarkable antibacterial activity may be associated with the phenolic compounds present in LCME, as phenolic compounds have been of considerable interest to humans because of their pronounced physiological, medicinal, and antibacterial properties²⁶. The inhibitory effect of LCME against three bacterial strains, viz. Escherichia coli (ATCC 10536), Klebsiella pneumoniae (ATCC 10031), and Bacillus subtilis (ATCC 11774) revealed that LCME had potent antibacterial effects against all the microorganisms studied. However, LCCE did not show any inhibitory effect on the microorganisms tested. The presence of phytoconstituents such as flavonoids, phenols, tannins, and other phytoconstituents in methanol extracts is known to have antimicrobial effects, which is why the difference in susceptibility of various test bacteria towards the extracts as observed in the study could be due to the nature of antimicrobial agents present in the extracts and their mode of action on the different test bacteria^27.

Phenolic compounds (phenolic acids, flavonoids, quinones, coumarins, lignans, and tannins) are the main free radical-scavenging molecules in ferns^28,29. Although limited studies have been carried out to determine the phenolic content of pteridophytes, comparison of the results is critical because of the various units used in conflicting studies. Edible fern Stenochlaena palustris contains 51.69mg g^-1 dry matter total polyphenol, 58.05 mg g^-1 dry matter flavonoids, and 48.80mg g^-1 dry matter hydroxycinnamic acids^30,31. Also, a polyphenols content of 2340mg GAE 100 g^-1 FW(Fresh weight) in Dryopteris filix-mas and 887.0mg GAE 100 g^-1 FW in D. affinis have been reported. A study carried out in Tunisia reported phenolic contents of ethyl acetate extracts ranging from 49.3 to 55.4mg GAE g^-1 in two ferns, Asplenium adiantum-nigrum and Asplenium trichomanes.³²

Flavonoids are a class of secondary plant metabolites with significant antioxidant and chelating attributes³³ and the Chloroform and methanolic extracts of L. cernua contain a high amount of total flavonoids, which correlates with the intense antioxidant activity of these extracts. Antioxidant activity may be due to the presence of phenolic hydroxyl or methoxyl groups, flavone hydroxyl, keto groups, free carboxylic groups, quinones, and other structural motifs^34,35. Several reports have conclusively correlated antioxidant activity with the amount of total phenolics/total flavonoids^36,37. The DPPH radical scavenging capacity was determined at several concentrations of extract ranging from 10-100 µg ml^-1 of the plant extract. The DPPH free radical scavenging capacity of the extracts increased with increasing extract concentration. Similar to the results obtained in the present study, many studies have confirmed the radical-scavenging and antioxidant properties of pteridophytes. Polystichum aculeatum showed significant antioxidant properties with an IC50 value of 0.45±0.02μg ml^-1 ³¹. Fern Asplenium trichomanes ethyl acetate extract exhibited the antioxidant activity, DPPH IC50 as 0.59±0.05mg ml⁻¹ ³². Therefore, it is remarkable that the pteridophyte evaluated in the present study showed a much higher radical scavenging capacity than those reported in previous studies. The presence of these compounds and their chemical structures can provide more detailed insights into the potential biological activity and medicinal properties of plants. Based on this study, most of these bioactive compounds have been proven to exhibit pharmacological potential.

5. CONCLUSION:

The screening of L.cernua plants extracts revealed the presence of major bioactive compounds. The investigation of these compounds will lead to the determination of the health benefits of plants. The extracts of L. cernua (L.) Pic. Serm. contains phytoconstituents that can be subjected to further studies. In addition, a notable inhibition zone was found when tested against three bacteria, which showed their potency as a contender for the antibacterial drug. A notable amount of phenols and flavonoids has been found, and the presence of a high amount of phenols may contribute directly to their antioxidant properties³⁸. Numerous investigations on the antioxidant activity of plant extracts have confirmed a strong linear correlation between phenol concentration and antioxidant activity ^4,39. The scavenging activity of L. cernua extract was exceptional compared to that of the standard, implying that the plant is a potential radical scavenger.

6. AUTHOR CONTRIBUTIONS STATEMENT:

The authors confirm contribution to the paper as follows:

1. Study conception, design, data collection analysis and interpretation of results: R. Vanlalpeka

2. Analysis and interpretation of results: Elizabeth Vanlalruati Ngamlai, Vanlalhruaii Ralte, P.C. Vanlalhluna.

3. Draft manuscript preparation: SK Mehta.

All authors reviewed the results and approved the final version of the manuscript.

7. CONFLICT OF INTEREST:

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest or non-financial interest in the subject matter or materials discussed in this manuscript. The authors have no financial or proprietary interests in any material discussed in this article.

8. ACKNOWLEDGMENT:

The authors would like to express their gratitude to Prof. K. Lalchhandama, PB. Lalthanpuii, and Zarzoliani for their invaluable assistance and contributions. Also, we would like to express our heartfelt gratitude and appreciation to the Ministry of Tribal Affairs for their financial assistance through the NFST.

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Received on 31.07.2023 Modified on 11.12.2023

Research J. Pharm. and Tech 2024; 17(5):2385-2390.

DOI: 10.52711/0974-360X.2024.00373