Assessment of Nutrient Composition and Antioxidant Activity of Some Popular Underutilized Edible Crops of Nagaland, India ()
1. Introduction
Underutilized edible plants are under exploited of its potential for contributing to food security (nutritional/medicinal), income generation and environmental services [1]; they are locally abundant instead of globally, lack scientific knowledge concerning their physiological, agronomic and ecological properties and have a limited current use relative to their economic potential. They have the potential to fight against poverty and starvation faced by many developing countries and can help promote crop diversification to encounter such problems and also improve the rural economy [2] [3]. Though they are not significant in terms of global production and consumption systems but are rich in macronutrients and micronutrients and comparatively they require relatively low inputs thereby contributing to rural sustainable agricultural production and combating the “hidden hunger” caused by micronutrients deficiencies [2] [3] [4] [5]. They have the capability to deliver many health benefits apart from fulfilling physiological needs and had been conferred the status of functional foods [6].
A diet rich in higher antioxidant activities with free radical scavenging molecules (flavonoids, anthocyanins, cartenoids, and dietary glutathionine), vitamins and endogenous metabolites can protect the human body against cellular oxidation reactions, cardiovascular events, cancer, and other age-related degenerative diseases [7] [8] [9]. Fruits, nuts and vegetables play a significant role in human nutrition especially as source of vitamins, minerals and dietary fiber [10]. They offer advantages over dietary supplements because of low cost and wide availability; as such they remain an important source of nutrients in many parts of the world. Nuts are good source of essential fatty acid, fiber, vitamin E and mineral [11]. Some components of fruits and vegetables are strong antioxidants and function to modify the metabolic activation and detoxification/disposition of carcinogens or even influence processes that alter the course of the tumor cell [12]. A high dietary intake of fruits and vegetables is strongly associated with a reduced risk of developing some chronic diseases, such as various types of cancer, cardiovascular disease, type II diabetes and other degenerative or age-related diseases, which causes death in many developed countries was established by clinical trial and epidemiological studies [8]. With the advantages of medical science, people live longer and are faced with diseases that come along with age and illnesses such as cancer and diabetes mellitus [13]. The antioxidants from plant origin are beneficial compared to synthetic ones as they do not have any side effect/genotoxic effect [14] [15], further natural antioxidants are advantageous due to cost effectiveness and easy accessibility in the form of vegetables and fruits [16]. Data on epidemiological and in vitro studies strongly suggest that foods containing phytochemicals with anti-oxidation potential have strong protective effects against major disease risks [17] and natural antioxidants in fruits and vegetables have gained increasing interest among consumers and the scientific community because epidemiological studies have indicated that frequent consumption of natural antioxidants is associated with a lower risk of cardiovascular disease and cancer [18]. Potential sources of antioxidant compounds have been searched in several types of plant materials such as vegetables, fruits, leaves, oilseeds, cereal crops, barks and roots, spices and herbs, and crude plant drugs [19]. Phenolic substances such as flavonoids are the most common compounds in fruits and vegetables and have strong antioxidant capacity [20] [21]. Crop improvement has played important role in sustaining and strengthening food and nutrition, health and livelihood in the world from the very beginning of domestication yet millions of people are still under-nourished [22] [23].
Nagaland, a small state of North-Eastern region of India very rich in its flora and fauna. Being a part of Indo-Burma biodiversity hotspot, the region is a home for unique biodiversity and the indigenous Naga tribes depends greatly on forest products as food source and is an integral part of their daily lives [2] [3]. Nagaland is basically an agricultural based state and cultivation of cereal crops plays a big part in agricultural system of the state. Millets and jobs tear are important traditional Naga cereal crops which have been passed down from generation through traditional preservation method. Forest has a large and indispensable role in improving the food security and livelihood of the tribal society [24]. About 70% of ethnic tribes are living in rural hilly areas and depends on minor forest products for livelihood including food and medicines. During 2012-16 three hilly districts (Kohima, Phek and Tuensang) of Nagaland, India was surveyed for underutilized wild edible plant species and 142 species were collected, documented [3]. Of these 142 species, 22 species were found to be popular among the tribal population. Following documentation, an attempt was made to understand the nutritional properties of these 22 popular underutilized edible plants (UEP).
2. Materials and Method
2.1. Survey Areas
Kohima District: Kohima is the capital city of Nagaland state, India, located between the geographical coordinates of 25.6701˚N and 94.1077˚E surrounded by the Dimapur district to the west, Phek and Zunheboto district to the east, Wokha district to the north and Manipur state to the south with a total geographical area of 1463 sq. km and an average elevation of 1444 m (4738 ft) above sea level. It is the home land of the Angami Naga tribe and agriculture is the main occupation.
Phek district: Phek district lies in the South-East of Nagaland with geo-graphical coordinate of 25.40˚N and 94.28˚E, bounded by Kohima district in the west, Zunheboto and Kiphire districts in the North, Myanmar in the South East and Manipur state in the South with an area of 2026 sq∙km. The district is inhibited by the Chakhesang Naga tribe and Puchury tribes with agriculture being the main occupation where 80.84% of the population engaged in agriculture and Terrace rice cultivation.
Tuensang District: Tuensang district is the largest district of Nagaland with geographical coordinate of 26.14˚N and 94.49˚E sharing an international border with Myanmar all along its eastern sector and is bounded by Mon district in the north east, Longleng in the north, Mokokchung in the south. Chang, Sangtam, Yimchunger and Khiamniungan are the main indigenous tribes of the district and Jhum-shifting cultivation is the main agricultural practice of the district.
An extensive field survey was carried out in different seasons during the period 2012-2016. With the help of forest experts and field guides, random collection of plant materials was carried out in study area during the different seasons of the year and also at the peak seasons of the plants. The collected plant materials were then kept in zipper poly bags and brought to the laboratory for identification and carry out nutritional studies.
2.2. Sample Preparation
The 22 selected UEP considered for the assessment consists of 2 cereal crops (Coix-lcrymajobi and Setariaitalica), 9 leafy vegetables (Centallaasiatica,Clerodendrum glandulosum, Elatostema platyphyllum, Lasiaspinosa,Polygonum chinense, Polygonum molle, Trichodesmakhasianum,Plantago erosa,Zanthoxylum oxyphyllum) and 11 fruits and nuts (Actinidia callosa, Hodgsoniamacrocarpa, Ficus auriculata, Ficus semicordata, Juglans regia, Olax imbricata, Phyllanthusemblica,Rhus chinensis, Spondias pinnata, Stixis suaveolens, Terminalia chebula). Fresh plant samples were harvested during right harvesting period in different seasons from the districts of Kohima, Phek and Tuensang and brought to the laboratory. The plant samples were rinsed with water, air dried and grounded into powder for the assessment. Thereafter, the prepared samples were subjected to analysis for nutritional and phytochemical content and antioxidant properties using different analytical methods. Details of the 22 selected UEP are listed in Table 1 along with the botanical name, common name and the parts used of the plants.
3. Nutritional Analysis
3.1. Proximate Composition
Moisture content: Moisture content was estimated following Association of Official Agricultural Chemists [25] method with slight modification. Two g of the collected each sample was taken in a separate pre-weighed dish and oven dried at 70˚C for ~4 h for leafy vegetables and ~18 h for fresh fruits, nuts and cereals. The moisture content was calculated by using the formula.
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Table 1. Twenty two selected underutilized edible plants for nutrient composition assessment.
Protein content: Protein estimation was determined by using the Colorimetric method described by Lowry [26]. About 500 mg of the oven dried sample was grounded and homogenized with 10 ml of 0.1M Phosphate buffer (pH 7.4) and centrifuged the solution at 1000 rpm for 10 min. The supernatant was filtered with Whatman filter paper and the filtrate was used for protein analysis. Pipette out 1 ml of the extract to which 5 ml of the Lowry’s regent was added. Mixed the solution well and allowed the mixture to stand for 10 min. Added 1N of Folin-ciocalteau reagent to the solution followed by incubation at room temperature in the dark for 30 min. Absorbance was taken at 660 nm and the standard curve was prepared with Bovine Serum Albumin.
Total carbohydrate: Total carbohydrate was estimated using the Phenol-Sulphuric Acid Method [27]. About 300 mg of sample was weighed and hydrolyzed by keeping it in a boiling water bath for 3 h with 5 ml of 2.5N HCl and cool to room temperature. The volume was made to 50 ml with distilled water and centrifuged at 1000 rpm for 10 min and the supernatant was filtered and the filtrate to be used for the estimation of total carbohydrate. To 1 ml of the extract, added 1 ml of 5% Phenol solution followed by 5 ml sulphuric acid (96%) and mixed well by shaking for 10 min. The content of the tube was placed on a water bath 25˚C to 30˚C for 20 min and the absorbance was read at 490 nm and the standard curve was prepared using glucose.
Reducing sugar estimation: Reducing sugar was estimated using the method of 3,5-dinitrosalicylic acid reagent [28]. One g sample was weighed and grounded with 10 ml of ethanol (80%, v/v) and the solution was centrifuged at 1000 rpm for 10 min, supernatant was then filtered and the filtrate was used for estimation of reducing sugar. To 1 ml of extract 3 ml of DNS reagent was added followed by heating the solution in a boiling water bath for 5 min. Added 1 ml of 40% (w/v) Rochelle salt solution (Potassium Sodium Tartrate) in the cooled reaction mixture. The absorbance was read at 510 nm and compared with the standard curve prepared using glucose.
Preparation of Sample extracts for Antioxidant activity,Total phenol content and Total flavonoid content: Methanolic extraction was prepared for estimation of antioxidant activity, total phenolic content, total flavonoid content. Ten g of dried sample was grinded in liquid nitrogen using mortar and pestle, powder was mixed with 100 ml of methanol and incubated for 24 h at 25˚C under continuous stirring at 150 rpm. The process repeated until the extraction solvent became colorless. The extract was then filtered on filter paper Whatman No. 4 and the filtrate was used for analysis.
3.2. Antioxidant Activity
DPPH Radical Scavenging Assay: 2, 2-Diphenyl-1-picrylhydazyl (DPPH) stable free radical method was used to determine the antioxidant activity of the plant extract following Aoshima et al. [29]. To 0.1 ml of sample extract with different extract concentrations (10 µg/ml, 50 µg/ml, 100 µg/ml, 150 µg/ml, 200 µg/ml), 2.9 ml of DPPH (0.1 mM DPPH prepared in methanol) was added and vortexed vigorously. Incubation of the reaction mixture for 30 min was done in the dark at 30˚C and the absorbance of the mixture was measured at 517 nm. Trolox was used as the standard for the evaluation of antioxidant activity. Inhibition of free radical by DPPH was calculated by the following equation:
Total phenolic content:The presence of polyphenols was determined by Folin-Ciocalteu method [30]. The resulting absorbance of the blue colored solution was measured at 765 nm and the total phenolic content of the mushroom samples were expressed as g of gallic acid equivalents (GAE) per g of the extract.
Total flavonoid content: The flavonoids content was estimated by spectrophotometric method following Sahreen et al. [31]. The absorbance of the solution was measured at 510 nm. Quercetin was used as the standard and the results expressed as g of quercetin equivalents (QE) per g of the extract.
3.3. Statistical Analysis
All the experiments were carried out in triplicate (n = 3) and data expressed as Mean ± Standard deviation.
4. Results
Proximate Analysis
Moisture content: Table 2 shows the moisture content of the 22 selected
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Table 2. Proximate quantification of different nutritional parameters of 22 selected underutilized edible plants.
*Data represents mean of three replicates (±Standard error).
plants varied significantly ranging from 4.8 to 88.15 g/100g. The maximum moisture content was recorded in the leafy vegetables which were recorded as 88.15, 85.6 and 84.9 g/100g in Plantagoerosa, Polygonumchinense and Elatostemaplatyphyllum respectively. The moisture content was significantly low in the nuts of Juglansregia recorded as 4.8 g/100g and also cereal crop Coix-lacrymajobi and fruit of Rhuschinensis showed very low moisture content which was recorded as 8.65 and 11.5 g/100g respectively. Over all, it was found that leafy vegetable samples have the highest moisture content (50.50 - 88.15 g/100g) compared to fruit samples (4.8 - 83.8 g/100g) and cereal crop (8.65% in Coix-lacrymajobi and 16.25 g/100g in Setariaitalica).
Protein content: Table 2 shows the protein content of the 22 plant sample varied significantly which ranged between 0.00269 - 0.773 g/100g of the sample (D/W basis). The maximum protein content was recorded in the fruits of Terminaliachebula (0.773 g/100g) which was followed by leaves of Polygonumchinense (0.54 g/100g) and fruits of Phyllanthusemblica (0.439 g/100g). The lowest protein content was recorded in the cereal crops Setariaitalica (0.00269 g/100g), Coix-lacrymajobi (0.00412 g/100g) followed by Ficusauriculata fruits(0.011 g/100g), Elatostemaplatyphyllum (0.013 g/100g) and Actinidiacallosa (0.026 g/100g). Over all, the 2 cereal crops showed the lowest protein content (0.00269 g/100g in Setariaitalica and 0.00412 g/100g in Coix-lacrymajobi) among the three group of the plant sample studied (Table 2).
Carbohydrate content: Table 2 shows the data of the present analysis that revealed, the carbohydrate content in the selected 22 plant samples shows significant variation ranging from 0.198 - 5.212 g/100g. The maximum carbohydrate content was recorded in Setariaitalica (5.212 g/100g) followed by Spondiaspinnata fruits (5.135 g/100g), Actinidiacallosa (5.135 g/100g) and seeds of Coix-lacrymajobi (4.379 g/100g) and lowest was recorded in the fruits of Juglansregia (0.198 g/100g) followed by nuts of Hodgsoniamacrocarpa (0.321 g/100g) and leaves of Lasiaspinosa (0.417 g/100g). Over all, the highest carbohydrate content was recorded in the cereal crops amongst the three groups of plants studied.
Reducing sugar: Unlike the other nutritional parameters, in Table 2 the value of reducing sugar content in the 22 plant samples studied does not vary much which ranges from 0.009 - 0.139 g/100g of sample. Reducing sugar content was highest in fruits of Ficusauriculata (0.139 g/100g) which was followed by fruits of Actinidiacallosa (0.097 g/100g) and leaves of Polygonummolle (0.081 g/100g). Seeds of Coix-lacrymajobi and Juglansregia (0.009 g/100g) were found to have the lowest reducing sugar content. It was established that the leafy vegetables and fruits content higher reducing sugar then the cereal crops. Table 2 shows the proximate composition of the 22 selected UEP with the parameters: moisture content, total carbohydrate, reducing sugar and protein content.
Antioxidant activity: Among the 22 UEP studied, maximum antioxidant activity was observed in Terminaliachebula fruits (37.49 µg/ml) followed by leaves of Clerodendrumglandulosum (65.29 µg/ml) and fruit of Phyllanthusemblica (79.08 µg/ml). The nut of Juglansregia (86.83 µg/ml), fruits of Rhuschinensis (84.73 µg/ml) and Spondiaspinnata (90.86 µg/ml) also showed very high antioxidant activity after Terminaliachebula, Clerodendrumglandulosum and Phyllanthusemblica extracts. The lowest antioxidant activity was observed in the seed of Setariaitalica (994.36 µg/ml), nut of Hodgsoniamacrocarpa (698.57 µg/ml) and seed of Coix-lacrymajobi (540.57 µg/ml). Figure 1-3, Table 3 shows the graphical representation of antioxidant activities of 22 studied UEP.
Total phenol content (TPC):The maximum TPC was recorded in the fruits of Terminalia chebula (53.11 mg GAE/g) and Rhuschinensis (43.99 mg GAE/g). The TPC value of T.chebula and R.chinensis varies significantly from the rest of the 20 plant samples as the value of TPC of the other samples which ranges from 0.09 mg - 8.75 mg GAE/g. The lowest TPC was recorded in the leaves of Elatostemaplatyphyllum (0.09 mg GAE/g) followed by the fruit of Ficusauriculata
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Figure 1. The antioxidant scavenging effect (% inhibition) of 2 cereal crops (Coix-lacrymajobi and Setariaitalica) at different extract concentrations against Trolox on DPPH radicals.
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Figure 2. The antioxidant scavenging effect (% inhibition) of 9 leafy vegetables at different extract concentrations against Trolox on DPPH radicals.
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Figure 3. The antioxidant scavenging effect (% inhibition) of 11 fruits and nuts at different extract concentrations against Trolox on DPPH radicals.
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Table 3. Quantification of total phenol content, Total flavonoid content and antioxidant activity of 22 selected UEP.
(0.82 mg GAE/g) and seed of Coix-lacrymajobi (0.84 mg GAE/g). Over all, the TPC of the selected plants samples are almost at the same level except for T.chebula and R.chinensis.
Total flavonoid content: The data revealed that the total flavonoid content (TFC) of the plant samples was much lesser than that of the TPC. The TFC from the leaves of Clerodendrumglandulosum (43.67 mg QE/g) and fruit of Terminaliachebula (27.78 mg QE/g) were found to be highest among the 22 plant samples. The TFC of the rest 20 plant samples does not showed much difference from each other as value ranges from 0.04 - 6.8 mg QE/g. The lowest TFC was found to be in the nut of Hodgsonia macrocarpa (0.004 mg QE/g) followed by the leaves of Elatostemaplatyphyllum (0.014 mg QE/g), fruit of Olaximbricata (0.02 mg QE/g), leaves of Plantagoerosa (0.04 mg QE/g) and seed of Setariaitalica (0.43 mg QE/g). Table 3 showed the proximate compositions of 22 selected UEP with the parameters: antioxidant activity, total phenol content and total flavonoid content.
5. Discussion
With increase in human population there is a growing concern about the food security throughout the world. Forest is an important source of various edible plants which are being used by rural populations throughout the world but their commercial potentials are not been exploited fully due to lack of data on different nutritional parameters. These plants/crops have the potential to fight against poverty and starvation of rural populations and developing countries. Many of the plant species are nutritionally rich, require relatively low investment for production and also contribute significantly in combating the “hidden hunger” and also deliver many health benefits [2] [3].
During present study 22 selected UEPs selected and different nutritional parameters varied significantly. The moisture content of Spondiaspinnata, Phyllanthusemblica, Setariaitalica, Ficusauriculata and Ficus semicordata in the present investigation are in agreement with the reports of Khomdram [32] [33], while moisture content of Hodgsoniamacrocarpa and Lasiaspinosa were lesser with the reports of Sundriyal and Sundriyal [34]. Report of moisture percent of Centellaasiatica (88%) by Rosalizan et al. [35] is higher than the present study (80%). Firdusi [36] reported the moisture content of Lasiaspinosa (86.30%) which comparative higher than the present study (50.50%). The reason for this difference could be due to stage and the time of collection of the sample.
Besides moisture content, other nutritional parameters were also investigated in these selected UEPs. In the present study the protein and reducing sugar content of Spondiaspinnata, Phyllanthusemblica, Hodgsoniamacrocarpa, Terminaliachebula and Zanthoxylumoxyphyllum were found to be much higher compared to findings of Khomdram [32] and Sundriyal and Sundriyal [34]. Protein quality of a food depends on its amino acid content and the physiological utilization of specific amino acid after digestion, absorption and minimal obligatory rates of oxidation [37] and that hydrolysis of protein occur during conversion of chloroplast to chromoplast which might have decreased protein content at ripening [38].
The present finding shows that antioxidant activity was higher in the fruit samples then leafy vegetables and cereal crop samples. Findings of Saha and Verma [39] shows higher antioxidant activity and TPC of T.chebula (14 µg/ml) and (13.4 g/100g) respectively but lower value TFC (0.793 g/100g) than the present study (antioxidant activity −37.49 µg/ml, TPC-53.11 mg/g, TFC-27.78 mg/g). Flavonoid and phenolic content shows better antioxidant activity, as such the maximum antioxidant activity was found to be Terminalia chebula, Rhuschinensis, Clerodendrumglandulosum, Juglansregia and Phyllanthusemblica which also showed the maximum content of Phenolic and/or Flavonoid. Findings of Chalise et al. [40] on T.Chebula,P.emblica and S.pinnata are higher than the present findings. Some factors such as habitat where the particular plant has been collected, time of harvesting, storage, ripening, drying and processing etc. may have affects on the antioxidant activity, TPC and TFC as suggested by Chaliseet al.
Nagaland with its diverse flora and its forest covering 12,966 sq. km is home to a large number of underutilized wild edible plants (leafy vegetable, fruit, nuts etc.). The present finding showed that some of the underutilized edibles plants are highly nutritious which are easily accessible and offers a cheaper option over inorganic commercial food products. The UEP were also found selling in local market in fresh form, dried form or roasted or made into a local product which cost around Rs. 20 - 50 per 400 - 500 gm packet and some are in high demand because of its taste, medicinal properties etc. [3]. Though the lifestyle and food habit of modern day has changed significantly with the advancement of Science and Technology, still over 70% of the population of ethnic tribes of Nagaland are living in rural areas with limited facilities and still depends on forest and forest products for food and health supplements/medicines. They mostly collect the vegetables, cereals etc from the forest for livelihood. These peoples have selected these lesser known forest products by trial and error methods over several generations without knowing the nutritional components. Present study is the first of its kind to know the nutritional parameters of some of the popular UEP of the region.
6. Conclusion
In the present investigation, assessment on the nutrient composition, phytochemical and antioxidant properties were carried out in 22 selected underutilized edible plants of Nagaland, India. The present investigation throws some light on the nutritional and antioxidant content of 22 selected underutilized edible plants which will help increase our knowledge on their use. The result from the present investigation can contribute as nutritional support to different region of the state for health improvement and help in development of the various value added local product of the underutilized edible plants which can help up-lift the socio-economic status of the local inhabitants of the state. Also, from the result obtained it was observed that many underutilized edible plants have high nutritional composition and antioxidant activity, it will be of great help if more research works are carried out in the future to study the phytochemical and nutraceutical properties of these plants which will help improve the present day medicine and its marketability.
Acknowledgements
The authors are thankful to Department of Biotechnology, Ministry of Science & Technology, Govt. of India, New Delhi, India for financial support through Institutional Biotech Hub vide order No. BT/22/NE/2011. Facilities used from the UGC-SAP (DRS-III) and DST-FIST programmes are duly acknowledged.