Review on Pseudo-Cereals of India

Abstract

Pseudo-cereals are non-grass, wild plants whose seeds are used in the same manner as cereals, but are underutilized due to the dominance of conventional cereal crops. Pseudo-cereals have varied adaptability. They are climatically more resilient and nutritionally richer than major cereal crops. They are enriched with essential amino acids and their protein content is either similar or greater than that of cereals. They contain adequate amounts of dietary fibers that help improve lipid metabolism. They also contain saponins, polyphenols, betalains, flavonoids, antioxidants, vitamins, and other important phytochemical compounds that help detoxify ROS and cope up with the diseases. Interest in the research of pseudo-cereals is growing among the research community due to its extraordinary nutritional and phytochemical profile and its potential in the development of gluten-free products. It can serve as an alternative food source against staple cereal crops under harsh environmental conditions and if cultivated sustainably, can resolve hunger issues in many countries. Pseudo-cereals form an integral part of the biodiversity due to its widespread usage by the tribals. Wild plants of many angiosperm families are used by tribal communities, but in this review, we will only focus on members of Amaranthceae and Chenopodiaceae families.

1. Introduction

Majority of the global population in present time is relying heavily on few major cereal crops such as wheat, rice, and maize for nutrition. These handful of crops are sustaining more than 50% of world population. Though they are rich in starch and are consumed for energy needs, they lack some essential micronutrients which has led to hidden hunger among the people. This micronutrient deficiency has affected nearly 2 billion people worldwide and has aroused serious health concerns [1]. This is not only affecting the human health but it also has adverse consequences on other plants such as pseudo-cereals whose biodiversity is declining due to the dominance of conventional cereal crops and for the same reason, they have remained underutilized till date. However, scientists have now turned their attention to the underutilized crops and they are showing considerable interest in pseudo-cereals because of their high resiliency towards the abiotic stress, nutritional, and phytochemical potential and their usage in gluten-free products. In near future, as the human population is predicted to rise, we will need to adopt an interdisciplinary approach to combat food crisis by not only improving the quality of available food by enrichment or biofortification but also by exploring other potential plants which are already enriched with required micronutrients which is an important aspect of food security [2].

Pseudo-cereals that we are going to consider in this review are dicotyledonous plants belonging to families Amaranthceae and Chenopodiaceae for example: Amaranthus viridis, Amaranthus spinosus, Achyranthes aspera, Celosia aregentea, and Chenopodium album. We will discuss their origin and distribution in brief, their characteristics and how they differ from cereals, their nutritional profiles, and processing techniques that makes them more palatable.

2. A brief of origin and distribution of pseudo-cereals

There are nearly 70 Amaranthus species under the family Amaranthceae out of which 17 species produces edible leaves and three species produces grains. A. viridis and A. spinosus might have originated from south and central America and today they are distributed over tropical and subtropical regions of Africa, South-East Asia, America, and in temperate Europe [3]. A. aspera is an herbaceous plant indigenous to Africa and Asia but is now found in nearly 60 tropical and subtropical countries [4]. Genera Celosia consists of 60 species all around the world. C. argentea is an erect, annual, herbaceous vegetable and is distributed in tropical and subtropical parts of the globe such as South Asia, Africa, and America [5, 6]. C. album belonging to the Chenopodiaceae family is an annual plant which is found in wild and is cultivated throughout India. Besides India, it is widely distributed in Europe, North America, Asia, and in different parts of Iran [7].

3. General characters and differences between pseudo-cereals and cereals

The grains of underutilized crops resemble to that of true cereals in functional aspect. However, they differ in nutritional and phytochemical aspects. Pseudo-cereal grains are composed of less of starch and more of proteins and lipids as opposed to cereals. The reason is, anatomically, pseudo-cereal grain contains lesser amount of endosperm (starch storing organ) and greater amount of embryo (that store proteins and lipids). Pseudo-cereals possess a considerable amount of essential amino acids such as lysine, cysteine, and methionine. Other than lysine, Amaranthus comprises of an adequate quantity of arginine and histidine which are inevitable nutrients for new born and children. Proteins in pseudo-cereals and cereals differ in their storage forms. In cereals, proteins are stored in the form of prolamins whereas in pseudo-cereals proteins are present in the form of globulins and albumins. High concentration of prolamins in cereals is responsible for disease like celiac disease. Therefore, pseudo-cereals are being sought out as an alternative to cereals for gluten-free diet. Studies have shown that dietary fibers found in Amaranthus are approximately in the same range as that of wheat. Regarding vitamins and minerals, the value of thiamine content has been found to be greater in amaranth than in wheat. Riboflavin, vitamin-C, folic acid, and vitamin-E are also prominent in amaranth. It has been observed that gluten-free products and ultimately gluten-free diets are deficient in calcium, magnesium, and iron. Thus, richer calcium content in pseudo-cereals is relevant for the people suffering from celiac disease, osteopenia, and osteoporosis. Fats in pseudo-cereals are more than in cereals especially high unsaturated fatty acids (particularly linolenic acid) are characteristic of pseudo-cereals. Amaranthus contains “squalene” which is a highly unsaturated, open chain triterpene which is exclusively found in the liver of deep-sea fish and other marine species. Lipid content is two to three times higher in pseudo-cereals than in cereals. This highly unsaturated lipids are also stable against oxidation which is a desirable trait. This feature is accredited to the tocopherols existing in relatively higher amounts [8]. In cereal grains, there are some anti-nutrients such as phytate, tannins, and saponins that interfere with nutrient absorption and utilization which are found in comparatively lesser quantities in pseudo-cereals. Hence, their nutrient profile makes them a suitable candidate for gluten-free products and are therefore in high demand among the consumers around the world, mainly among the celiac disease patients. This high caloric content and balanced amino acids in pseudo-cereals are advantageous to cope up with micronutrient deficiency in developing and under-developed countries [9].

A. viridis and A. spinosus are an excellent source of protein with lysine and methionine and phytochemicals such as carotenoids, ascorbic acid, dietary fibers, and minerals such as Ca, Mg, K, P, Fe, Zn, Cu, and Mn. They are an impressive source of antioxidants and vitamins which is why they have great importance in food industry. They are consumed as cooked, steamed, or fried vegetables [3].

A. aspera is an important source of biologically active trace elements and metals. It is rich in Fe, Cu, Ca, and Na [10]. Leaves of A. aspera predominantly comprises of fats, saponins, flavonoids, alkaloids, and tannins. These phytochemicals, especially phenolic compounds are responsible for the harmful ROS scavenging property of the plant that makes it a potential source of human nutrition [11].

In the extracts of Celosia argentea, the characteristic phyto-constituents determined were cyclic peptides, phenols, saponins, amino acids, flavonoids, alkaloids, and tannins. Saponins among all are the principal pharmacologically active agents but are needed to be explored further for their bioactivity and usefulness. Apart from saponins, higher concentration of fats renders the plant eligible as an energetic and nutritional candidate for mal-nourished children [12, 13].

The determination of vitamin-C and β-carotene from the young as well as mature shoots of C. album indicated that it can serve as an interesting supplement of vitamins in the diet bowl. Also, there were prominent amounts of nutrients such as proteins, crude alkaloids, and saponins along with elements like potassium, calcium, zinc, and iron but on the contrary, dietary fibers were little less. All the above-mentioned components have beneficial impact on our health [14].

4. Nutritional profile

This section deals with the nutritional aspect of chosen A. viridis, A. aspera, and C. album in context of their protein, carbohydrate, fat, dietary fiber, and vitamin and mineral composition. Nutritional composition of major cereals, that is, wheat, rice, and maize are incorporated for comparative study (Tables 1–7).

4.1 A. viridis

Nutrients	Concentration (g/100 g)
Protein	14.95 ± 0.19^c
Fat	6.30 ± 0.05^a
Total sugars	0.27 ± 0.01^b
Soluble fiber	0.68 ± 0.01^c
Insoluble fiber	29.92 ± 0.01^d
Carbohydrates	28.55 ± 0.76^a
Essential minerals	(mg/g)
Calcium (Ca)	5.97 ± 0.27^d
Potassium (K)	6.66 ± 0.19^c
Magnesium (Mg)	4.27 ± 0.02^d
Sodium (Na)	0.77 ± 0.01^d
Phosphorous (P)	8.73 ± 0.02^a
Trace elements
Iron (Fe) (mg/g)	0.33 ± 0.23^a
Chromium (Cr) (μg/g)	5.36 ± 0.01^b
Copper (Cu) (μg/g)	6.14 ± 0.01^b
Zinc (Zn) (μg/g)	24.95 ± 0.01^b

Table 1.

Chemical composition of Amaranthus viridis (grains) in dry basis [15].

Average followed by different letters on the same line indicate statistical difference according to the Duncan test (p ≤ 0.05).

4.2 A. aspera

Nutrients	Concentration (g/100 g)
Crude protein	36.71
Crude fat	8.31
Carbohydrates	37.52
Crude fiber	0.44

Table 2.

Proximate chemical composition of Achyranthes aspera (seeds) in dry basis [16].

Minerals	Concentration
Macro-minerals	(mg/g)
Sodium (Na)	0.06 ± 0.01^b
Potassium (K)	6.35 ± 0.04^b
Calcium (Ca)	0.17 ± 0.01^b
Magnesium (Mg)	2.18 ± 0.01^b
Trace minerals	(μg/g)
Molybdenum (Mo)	0.28 ± 0.02^b
Manganese (Mn)	30.20 ± 0.63^b
Aluminum (Al)	41.07 ± 4.16^b
Iron (Fe)	76.82 ± 4.15^b
Zinc (Zn)	41.77 ± 0.18^a
Copper (Cu)	7.67 ± 0.19^b
Strontium (Sr)	3.39 ± 0.26^b
Cadmium (Cd)	0.10 ± 0.04^b
Lead (Pb)	0.21 ± 0.02^b
Ultra-trace minerals	(μg/g)
Chromium (Cr)	2.18 ± 0.38^b
Cobalt (Co)	0.09 ± 0.01^b
Nickel (Ni)	1.35 ± 0.44^b
Tin (Sn)	0.18 ± 0.04^b

Table 3.

Mineral composition of Achyranthes aspera seeds (dry powder) [17].

Means (±SEM) sharing different letters in the same row are significantly (P < 0.05) different (n = 3).

4.3 C. album

Nutrients	Concentration (g/100 g)
Protein	13.12^b ± 0.07
Fat	6.50^a ± 0.30
Crude fiber	13.09^b ± 0.04
Carbohydrate	54.61^a ± 0.09
Total starch	41.44^a ± 0.29

Table 4.

Proximate composition of Chenopodium album (flour) [18].

Mean values in the same row which is not followed by the same letter are significantly different (p < 0.05). Values represent mean ± standard deviation (n = 3).

Minerals	Concentration (mg/kg)
Calcium (Ca)	177.89^a ± 4.04
Sodium (Na)	82.45^b ± 0.42
Iron (Fe)	112.07^a ± 1.26
Magnesium (Mg)	1600.34^a ± 15.01
Copper (Cu)	5.90^b ± 0.36
Zinc (Zn)	24.20^b ± 0.23
Potassium (K)	10113.31^a ± 21.50

Table 5.

Mineral composition of Chenopodium album (flour) [19].

Mean values in the same row which is not followed by the same letter are significantly different (p ≤ 0.05). Values represent mean ± standard deviation (n = 3).

4.4 Zea mays (maize), Triticum aestivum (wheat), and Oryza sativa (rice)

Cereals	Protein	Fat	Fiber	Carbohydrate
Wheat	12.39 ± 0.010	2.50 ± 0.010	1.14 ± 0.070	75.65 ± 0.240
Maize	8.58 ± 0.000	2.85 ± 0.020	2.83 ± 0.020	75.39 ± 0.030
Rice	10.49 ± 0.010	3.94 ± 0.030	1.09 ± 0.000	75.61 ± 0.450

Table 6.

Proximate composition (%) of cereals [20].

Values reported were average of duplicate analysis.

Cereals	Wheat	Maize	Rice
Sodium (Na)	383.33 ± 0.001	333.33 ± 0.0011	126.67 ± 0.001
Potassium (K)	416.67 ± 0.001	300.00 ± 0.001	183.33 ± 0.001
Calcium (Ca)	60.02 ± 0.0027	12.95 ± 0.7770	3.35 ± 0.0019
Magnesium (Mg)	140.73 ± 0.0053	77.62 ± 0.0037	23.67 ± 0.0052
Iron (Fe)	67.22 ± 0.0011	58.35 ± 0.0006	59.33 ± 0.0005
Zinc (Zn)	11.73 ± 0.0011	9.45 ± 0.0009	9.27 ± 0.0006

Table 7.

Mineral composition (mg/100 g) of cereals [20].

Mean ± standard deviation.

5. Processing treatments for pseudo-cereals

Their extraordinary nutritional profile is the result of the presence of countless bioactive components that includes essential amino acids, proteins, phenolic compounds, and a wide range of anti-oxidants, thus rendering them with a high nutraceutical potential. But along with favorable substances, they also contain anti-nutrients such as phytate, tannins, and saponins which reduces the bioavailability of beneficial supplements. To resolve this, pseudo-cereals are subjected to several processing treatments like soaking, fermentation, popping, germination, and cooking. Such treatments improve bioavailability of nutrients by decreasing the amount of anti-nutrients and consequently enhances the nutritional value of pseudo-cereals. For example, seeds of Amaranthus are consumed as popped, sprouted, baked, or grounded into flour and cooked as porridge [21].

5.1 Processing treatments

Processing increases the digestibility and palatability of respective food product. It extends the self-life and reduces the anti-nutritional compounds. Following are few traditional methods for processing pseudo-cereals to make them more consumable.

5.1.1 Fermentation

Fermentation is a metabolic process carried out by anaerobic microorganisms in which carbohydrates are broken down to release energy. It is an age-old technique for food preservation. Pseudo-cereals are an adequate source of carbohydrates, minerals, vitamins, sterols, and other growth factors that sustains the microbe populations. These grains are composed of an indigenous microbiota comprising of molds, lactic acid bacteria (LAB), enterobacteria, etc. LAB are gram positive, strictly fermentative bacteria which carries out lactic acid fermentation and produces lactic acid as the major metabolic end product of carbohydrate fermentation and the most frequently used strain for this purpose is Lactobacillus plantarum.

Lactic acid fermentation is a commonly used food processing technique which can be employed in many different ways to improve nutritional and functional quality of pseudo-cereals such as production of bioactive peptides to stimulate immune system, increasing total phenolic content and antioxidant capacity, decreasing of anti-nutritional factors like phytic acid, tannins, and enzyme inhibitors. The formation of lactic acid during fermentation leads to a decrease in pH that results in enhanced activity of endogenous phytase. Phytases constitutes particular subgroup of phosphatases which are responsible for lowering or eliminating the anti-nutritional effect of phytic acid. Some LAB strains and other vitamin producing microorganisms can elevate the concentrations of natural form of vitamins that leads to the decrease in side effects of chemically synthesized vitamins. Hence, they can be utilized as an alternative source of biofortification which is also a cost-effective strategy and eliminates the need to add synthetic vitamins. Food products consumed after fermentation with LAB improves the overall nutritional quality by increasing vitamin B9 concentrations. There is a need to explore more beneficial effects of lactic acid fermentation to design novel and healthier edibles especially for patients with celiac disease [22, 23].

5.1.2 Popping

Also known as heat induced puffing, is a low-cost technology in which heating at atmospheric pressure gives rise to high internal pressure due to evaporation of moisture, causing the pericarp to break, leading to the expansion of endosperm. Puffed grains undergo dehydration as well as structural and textural changes. Puffing increases digestibility and functionality of the grains. Because of such modifications, Amaranthus flour has been proposed to be used as an ingredient in bakery products. Puffed grains are ready-to-eat products, also incorporated in the snack formulations [24].

5.1.3 Germination

Germination is a process in which a new plant arises from the seed if the seed is under favorable conditions. Imbibition is the first step in germination process in which the dry seed absorbs water which leads to the increased metabolic rates and subsequent growth. The interesting part is the rise of hydrolytic enzyme activities followed by breakdown of stored macromolecules in the seed. Such changes alter the technological properties and functionality of grains which is a desirable asset. During germination, the action of hydrolytic enzymes on starch increases its digestibility. It also increases the content of free amino acids which are readily absorbed compared to the intact proteins, influencing the postprandial protein metabolism. The breakdown of cell wall changes the solubility of fiber components and increases the amounts of bioactive compounds and antioxidant activities [25].

5.1.4 Cooking

Grains of pseudo-cereals are generally eaten after boiling. However, excessive boiling decreases the phenolic contents of the grains. Highest retention of phenolic contents was observed by pressure cooking. From anti-nutritional aspect, no significant reduction was seen in anti-nutritional compounds, especially of phytic acid through boiling. Evaluation of minerals in Amaranthus revealed that boiling and steaming negatively affected the folate content and also certain essential amino acids [26].

6. Conclusion

Pseudo-cereals are a powerhouse of nutrients. There is a need to explore them further and bring them in our daily diet. Even though pseudo-cereals seem more superior than cereals in context of their chemical composition, the anti-nutrients present in them reduces the bioavailability of the nutritional components. Phytate and lower inositol phosphates binds to the minerals like calcium, zinc, magnesium, and iron, making them unavailable for absorption [26]. As nutritional deficiency is becoming more prevalent among the human population throughout the globe, food producers are expected to develop novel strategies for their improved processing. Moreover, there is a requirement of making people aware about the benefits of pseudo-cereals so that they consider them in their diet along with the cereals which will also elevate the nutritional quality of their diet. Prerequisite for this is to design new range of food products prepared using pseudo-cereals as their key ingredients and introduce them into the market. Pseudo-cereals are also in demand for the manufacture of gluten-free edibles. Therefore, it is very important to have a detailed understanding of the properties of pseudo-cereals and their benefits and drawbacks. This will aid in boosting the quality of life of the people with celiac and other gluten-induced diseases. Pseudo-cereals have an immeasurable potential, the only task is to give an eye to them.

Acknowledgments

Thanks to the head of the Department of Botany, Faculty of Science, The Maharaja Sayajirao University of Baroda for providing laboratory facilities at the department.