Abstract
Moringa (Moringa oleifera Lam.) is a widespread multipurpose tree with great potential as a high-value crop for its nutritive, therapeutic and prophylactic properties with several industrial applications. Almost every part of the tree is useful with varied end uses. It is an interesting plant owed to its bioactive compounds. Moringa species have been widely spread across the tropical and subtropical regions of the world and a total of 13 species of the genus Moringa are known. Moringa, being a cross-pollinated tree, high heterogeneity in many character forms is observed resulting in vast genetic diversity in the natural and cultivated accessions and substantial variation in quantitatively inherited traits has been documented which needs to be exploited for concentrated research towards its crop improvement. In-depth knowledge and understanding of the gene flow pattern and population genetic structure in moringa through molecular genetic diversity and population structure of worldwide collections is of great promise. In spite of its varied uses and morphological diversification, the number of accessions collected as germplasm and their conservation in gene banks is very meagre. Documentation of genetic diversity and conservation of germplasm is a necessity for strategic research as well as breeding programmes to develop elite varieties. This chapter highlights the genetic diversity in moringa, its significance in the contemporary nutritional security scenario and its exploitation for future programs.
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7.1 Introduction
Moringa (Moringa oleifera Lam.) is a widespread multipurpose tree known for its nutritive, therapeutic and prophylactic properties with numerous industrial applications. It is an ancient seldom utilized tree but gaining importance recently due to its exceptional uses. It is being studied for nutritional attributes and as a livestock fodder crop. The fast-growing ability of the crop helps to withstand both severe drought and mild frost conditions and has made moringa, a hardy tree crop cultivated wildly across tropics and subtropics (Csurhes and Navie 2016). Globally, moringa is being promoted as a nutritious tree crop in marginal areas with less rainfall as well as homestead gardens (FAO 2020). This tree has the prospective to increase nutrition, food security and boost rural development (Hsu et al. 2006). The long, slender, triangular seed-pod properties earned it the vernacular name ‘drumstick tree’ and from the horseradish taste of the roots ‘horseradish tree’ besides, ben oil tree or benzolive tree (Paliwal et al. 2011). It is popularly called as ‘mother’s best friend’ in the Philippines, as it is consumed to increase a woman’s milk production as well as for the treatment of anaemia (Estrella et al. 2000; Siddhuraju and Becker 2003). Recently this species has been dubbed as ‘miracle tree’ or ‘natural gift’ or ‘mother’s best friend’ (Leone et al. 2015; Pirro et al. 2019).
Almost every part of the tree is useful either for its nutritional value or for commercial purposes, hence, it is also known as the ‘natural nutrition of the tropics’. The leaves, flowers, fruits and immature pods are highly nutritious and consumed in Asian, African and American countries such as India, Pakistan, Sri Lanka, Burma, Indonesia, Philippines, Hawaii (Anwar and Bhanger 2003). The extracts from moringa leaves are used to treat malnutrition, augment breast milk in lactating mothers as they are rich in minerals, vitamins and other essential phytochemicals. It has the potential to use as an antioxidant, anticancer, anti-inflammatory, antidiabetic and antimicrobial agent. Moringa seed is extensively used in the purification of drinking water as it acts as a natural coagulant (Gopalakrishnan et al. 2016; Falowo et al. 2018). In various forms, this tree is used to treat turbid water in many countries (Suarez et al. 2003; Bhatia et al. 2007). In addition to food uses, moringa is being used for animal feed (Sánchez et al. 2006). When supplemented to the diet of dairy animals, moringa leaves improve dry matter intake, digestion and milk production, but without affecting the smell, taste or colour of milk (Sánchez et al. 2006). Further, leaf and seed powders are a good source of phytomedical compounds (Anwar et al. 2007). It is also a promising source for bioenergy (Adu-Dapaah et al. 2015).
7.2 Origin and Distribution
Moringa species have been widely spread across the tropical and subtropical countries of the world (Csurhes and Navie 2016). Moringa is thought to originate from northern India, specifically around Agra and Oudh and South of the Himalayan Mountains (Vogt 1996). It spread to eastern Africa during the beginning of the twentieth century (Mallenakuppe et al. 2015). The species is either grown commercially or present in wild across Asian, African, North American, Central American, the Caribbean, South American and Oceania counties (Acevedo-Rodríguez and Strong 2012). In recent times, Moringa is being grown throughout the Middle East, almost the whole tropical belt and is expanding to a diverse environment of tropical and subtropical regions in Africa and America (Pandey et al. 2011; Chang et al. 2019).
7.3 Genetic Resources of Moringa
Moringa belongs to the order Brassicales and the monogeneric family Moringaceae, which consists of about 33 species (Arora et al. 2013). Among these, 13 species, viz., M. arborea, M. longituba, M. pygmaea, M. concanensis, M. borziana, M. hildebrandtii, M. stenopetala M. oleifera, M. ovalifolia, M. peregrina, M. rivae, M. drouhardi, M. ruspoliana are found worldwide (Stephenson and Fahey 2004). Origin of moringa species could be traced back to different countries: M. arborea, native to Kenya; M. borziana from Somalia and Kenya; M. rivae and M. stenopetala originated from Kenya and Ethiopia; M. pygmaea native to Somalia; M. longituba from Ethiopia and Somalia; M ruspoliana native to Ethiopia; M. ovalifolia from Namibia and Angola; M. drouhardii and M. hildebrandi from Madagascar; M. peregrine from Red Sea and Horn of Africa; M. concanensis and Moringa oleifera indigenous to sub-Himalayan tracts of northern India, among which Moringa oleifera has been the most well-studied and used species for human consumption (Paliwal et al. 2011). Further, M. arborea, M. ruspoliana, M. longituba, M. stenopetala M. rivae, and M. borziana are in danger of extinction (Stephenson and Fahey 2004). Only M. oleifera is cultivated (Sánchez et al. 2006). Moringa cytological studies revealed that Moringa oleifera has 2c genome size of 1.2 pico gram (pg) (Ohri and Kumar 1986). The diploid chromosome number of this species is 2n = 28 (PROTA 2017).
Distribution of several ecotypes can be seen across India with several vernacular names, namely; Jaffna and Chavakacheri murungai (soft and taste fruits), Chemmurungai (red-tipped fruits), Kadumurungai with small and inferior fruits, Palmurungai and Punamurungai having a bitter taste, Kodikalmurungai with short fruit, wild Kadumurunga and Kodikkal Murungai (Kumar Ganesan et al. 2014). Two varieties viz., PKM-1; PKM-2 from Tamil Nadu and one variety, Bhagya from Karnataka, India, have been developed higher pod yield, pod quality and nutritional parameters. Several moringa varieties with desirable attributes also developed from Kerala, India (Kumar Ganesan et al. 2014). Even though vast variability is present as cultivated accessions and natural accessions, systematic studies towards the collection of wild and local forms as well as cultivated accessions across the globe and genetic diversity quantification are meagre. In spite of its varied uses and morphological diversification, the number of accessions collected as germplasm and their conservation in germplasm banks are just emerging across the world. The gap between the inherent genetic variability available and its poor representation in gene banks is a hindrance for crop improvement programs that needs to be addressed. So, gene/germplasm banks covering the entire genetic variability in Moringa is a necessity for concentrated research as well as breeding programmes to develop elite varieties.
Most of the genetic variation of M. oleifera is reported in India (Kumar Ganesan et al. 2014; PROTA 2017). The species has various cultivars, including some cultivated as annuals in temperate climates. DNA barcode details are available at the Barcode of Life Data Systems (Godino et al. 2015). Research centers concentrated on Moringa oleifera improvement across the globe are AVRDC (Taiwan), Moringa Philippines Foundation (Philippines), Moringa community (Zambia) and Rural development initiative (Zambia). Germplasm collections are stored at various facilities worldwide (Patricio and Palada 2015). The World Vegetable Center at Taiwan maintains collections of four moringa species, the majority of which are M. oleifera (Palada et al. 2017). Further, moringa collections are also maintained at the International Moringa Germplasm Collection in Mexico and Burkina Faso and the Philippines (IMGC 2017; PROTA 2017). The International Moringa Germplasm Collection houses living material of 12 of the 13 Moringa species at the Instituto de Biología, Universidad Nacional Autónoma de México (UNAM), Mexico (PROTA 2017).
7.4 Genetic Diversity in Moringa Oleifera
Genetic diversity is an essential pre-requisite in crop improvement. The chances of obtaining desirable transgressive segregants depend on the extent of parental genetic diversity: the greater the genetic diversity, the higher the prospects of desirable segregants. Diverse agro-ecological conditions, migration of genetic material due to genetic drift, gene flow, introduction/exchange of genetic stocks at national and international levels, along with adoptive as well as intensive artificial selection are responsible for the diversification of drumstick plants.
Moringa, being an outbreeding tree, high heterogeneity with high diversification in many characters are observed. The crop shows extensive diversity of morphological and biochemical properties, which serve as a resource for its genetic improvement (Godino et al. 2015). Wide variability was revealed like tree habit from deciduous to evergreen; shape of the tree varying from semi spreading to upright; flowering time wherein some trees flower throughout the year and some flower in two distinct seasons (Ramachandran et al. 1980; Raja et al. 2013) and resistance to hairy caterpillar (Mgendi et al. 2010; Raja et al. 2013).
Thirty-six genetically diverse genotypes of drumstick were clustered into five clusters based on the content of vitamin C, protein, nitrogen, phosphorous, potassium, calcium, iron and magnesium. The analysis used measures the forces of differentiation at two levels, namely intra-cluster and inter-cluster levels, and thus help in the selection of genetically divergent parents for exploitation in hybridization programmes (Tak and Maurya 2015). Genetic diversity, population structure and correlation in Indian populations of Moringa oleifera studied by Rajalakshmi et al. (2019) revealed the high variability existent at an intra-population level.
7.5 Nutritional Diversity in Moringa
Moringa is one of the most useful trees that can be used for food, nutraceutical value and industrial purposes (Khalafalla et al. 2010). People use its leaves, flowers and fresh pods as vegetables, while others use it as livestock feed (Anjorin et al. 2010). The significance of moringa to address nutritional deficiencies is based on the abundance of vitamins, minerals and protein found in the leaves and pods. These include vital nutrients such as beta-carotene, iron, zinc, vitamin C and all the essential amino acids (Moyo et al. 2011). The plant is rich in other bioactive and anti-inflammatory compounds like phenolics and isothiocyanates, while being relatively low in anti-nutrients (Falowo et al. 2018; Waterman et al. 2014). Different parts of the plant are differing with respect to their nutritional value. 100 g of pod yields 26 cal of energy; 2.5 g protein; 0.1 g fat; 3.7 g carbohydrates; 4.8 g fibre; 0.05 mg vitamin B1; 0.07 mg vitamin B2; 0.2 mg vitamin B3; 120 mg vitamin C; 30 mg calcium; 24 mg magnesium; 110 mg phosphorous; 259 mg potassium; 3.1 mg copper; 5.3 mg iron and 137 mg sulphur. Whereas, fresh leaves yield about 92 cal of energy and 6.7 g protein; 1.7 g fat; 12.5 g carbohydrates; 0.9 g fibre; 0.06 mg vitamin B1; 0.05 mg vitamin B2; 0.8 mg vitamin B3; 220 mg vitamin C; 448 mg vitamin A; 440 mg calcium; 42 mg magnesium; 70 mg phosphorous; 259 mg potassium; 0.07 mg copper and 0.85 mg iron (Gopalakrishnan et al. 2016). The leaves are considered as a better source of protein, Ca and Fe while the pods are rich in P, Na and Mg. Both the edible parts (leaves and pods) more specifically leaves have the potential to be used as micronutrient supplements for food products (Mallenakuppe et al. 2015).
The presence of wide nutritional variation in Moringa could be accredited to varying genetic backgrounds of the plant, in terms of ecotype, cultivar as well as environmental factors (Sánchez-Machado et al. 2010). Nutritional composition of four species; M. oleifera, M. peregrine, M. stenopetala, M. drouhardii indicated high overall nutritive value, antioxidants and glucosinolates, with low oxalate content, whereas M. oleifera contained the highest amounts of β-carotene, ascorbate, α-tocopherol, iron and protein content and M. peregrina was the uppermost for antioxidants (Yang et al. 2006). Substantial variation for chlorophyll, protein, macronutrient and micronutrient content in the leaves of different genotypes of M. oleifera and M. peregrina was revealed, which indicated higher chlorophyll in M. peregrine and higher protein content in M. oleifera (19.1–32.9%) than M. peregrine (12.5–24.6%).
Similarly, Fe and Zn contents varied between 250–490 ppm and 26.7–58.3 ppm respectively in M. oleifera versus 285–403 ppm and 15.7–38.9 ppm in M. peregrine. Mp genotypes were mostly intermediate in K content compared to Mo genotypes (1.3–2.0%). Calcium content in both species ranged from 0.03 to 1.3%. The highest Mg content was found in Mp genotypes (1.0%). Genotypes also varied in their content in Zn, Cu, and Mn for both species (Hassanein 2018). A similar trend of macronutrients was reported on M. oleifera genotypes grown in the Philippines (Magat et al. 2009). Further in Ghana, different genotypes of M. oleifera varied in protein and Ca contents with a wider range of protein, 26–27% in Ghana and significantly differed in their contents of all studied nutrients (Asante et al. 2014). Saudi Arabia M. oleifera genotypes were reported to be more diverse than those of other regions for their nutrient contents (Nouman et al. 2016).
Various accessions of moringa from different agro-ecological regions of Rajasthan, Uttarakhand, Uttar Pradesh, Madhya Pradesh and Goa have revealed high variability in the quantity of phytochemicals (Nouman et al. 2016). Two cultivars from the two ecological regions Chapai Nawabganj (L1) and Pabna (L2) of Bangladesh indicated a wide variation in nutritional value for protein and mineral nutrients viz., Ca, Fe, P and K. Ten moringa accessions, selected from a survey of 60 moringa accessions revealed variation for nutrient contents (Islam et al. 2020). Polyphenolics composition, antioxidant activity and contents of selected nutrients in the leaves from seven cultivars of M. oleifera (‘Tumu’, ‘Sunyaw’, ‘Kumasi’, ‘Techiman’, ‘China’, ‘Pakistan Black’ and ‘Pakistan White’) in Pakistan revealed variation among cultivars (Nouman et al. 2016).
7.6 Polymorphism and Allelic Frequency
Molecular diversity among seven populations of M. oleifera from Africa was explored and molecular variance of 59.15% between populations was inferred. When compared with the Indian population, African population showed 18.59% of variation existed between the two populations (Muluvi et al. 1999). These seven populations also revealed a total of 236 amplifications, of which 157 (66.5%) were found to be polymorphic between or within the populations (Muluvi et al. 1999). The microsatellite marker analysis of 24 germplasm of moringa exhibited an average of two to six alleles per locus. The expected and observed heterozygosity varied from 0.361 to 0.761 and from 0.01 to 0.875, respectively (Wu et al. 2010). Taxonomic analysis of 75 accessions of Moringa from Nigeria revealed a high level of polymorphism between the samples from south-central and northern parts of the country (Abubakar et al. 2011).
The high degree of polymorphism (74%) with respect to the genetic relationship was reported between the accessions from Brazil (da Silva et al. 2012). 161 accessions of M. oleifera from Asia, Africa, South and North America, and the Caribbean revealed allelic diversity of 8.3 alleles per SSR marker with a total of 158 alleles in 131 wild accessions collected from Pakistan and 30 accessions obtained from Florida (Shahzad et al. 2013).
Further, the genetic diversity in these 12 Indian populations using SSR primers elucidated a total of 35 bands of which 29 bands exhibited polymorphism (82.86%) with 1.84 bands /primer. Analysis of molecular variance (AMOVA) revealed 2% diversity which could be attributed to differences among regions, 3% at the level of populations and 95% contributed by the genotypes within the populations (Kumar Ganesan et al. 2014). A total of 74 alleles with a range of 4 to 15 were detected in 70 accessions of M. oleifera with an average of 7.4 alleles per locus. Allele frequency varied from 0.214 to 0.671 with a mean of 0.477; gene diversity from 0.487 to 0.885 with a mean of 0.669 while the average PIC value was 0.633 (Popoola et al. 2017). The genotypes collected from different countries revealed the presence of a higher genetic variance of 1.80 and 0.13 for the Malaysian population and 0.30 and 0.19 for the international population, respectively (Rufai et al. 2013).
Three molecular marker techniques, i.e. random amplified polymorphic DNA (RAPD), inter simple sequence repeat (ISSR) and cytochrome P450 gene-based markers in eight Indian cultivars of M. oleifera, revealed 48.68, 48.57 and 40.00% polymorphisms, respectively (Saini et al. 2013). Genetic variability analysis in 97 M. oleifera accessions indicated an average of 59.6% polymorphism through ISSR and 70.13% with SRAP markers. The mean gene diversity h (0.2), gene flow Nm (2.86) and a PhiPT value (0.14) estimated for the markers indicate the high variability existent at an intra-population level. Population structure results and cluster tree divided the samples into two groups: One group consists of Tamil Nadu accessions and the other comprises Andhra Pradesh and Odisha accessions (Rajalakshmi et al 2019). Figure 7.1 describes different factors that influence the Moringa genetic diversity.
Figure 7.1 Multiple factors affecting genetic diversity in a population of drumstick: Being a cross-pollinated crop, the genetic variability within and among the populations of moringa is derived from a wide assortment of genes and alleles which is affected by various factors. Mating patterns such as non-random outbreeding is common in cross-pollinated species. Random forces, such as population bottleneck causes changes in allelic frequency, which leads to genetic drift. Individuals within a population are subjected to spontaneous mutation, which evolves the species. Movement of individuals into or out of a defined location causes the migration of a set of alleles within a population. Natural disasters and competition for food and other resources favour certain individuals, naturally selecting them for further generations.
7.7 Principal Coordinate Analysis
Principal coordinate analysis (PCA) clusters and relates individuals or populations based on genetic distances. PCA of 20 genotypes of M. oleifera from different countries classified the twenty genotypes of Moringa into five major groups; two genotypes from Malaysia in one group. Dimension one of the PCA ranged from 0.49 to 0.92, while dimension two varied from −0.65 to 0.26 and dimension three varied from −0.65 to 0.68 (Rufai et al. 2013). PCA of 12 Indian populations of M. oleifera revealed very high genetic diversity in the Indian drumstick collection (Kumar Ganesan et al. 2014).
Phenotypic intraspecific variations among 40 accessions of M. oleifera collected from different agro-ecological zones of Nigeria revealed a high degree of intraspecific variability for reproductive characters. The first five principal component axes explained 61.40% of the overall variation with PC1 (23.92%) and PC2 (14.19%) contributing 38.11% of the total variation (Popoola et al. 2016). Commercially grown Moringa oleifera cultivars from India resulted in PCA plots where all the cultivars were assembled into four major clusters and genotypes belonging to a particular sub-cluster were grouped together (Saini et al. 2013).
7.8 Phylogenetic and Population Structure
In-depth knowledge and understanding of the detailed gene flow pattern and population genetic structure in Moringa is very meagre (Muluvi et al. 2004). Thus, the development of efficient molecular markers for M. oleifera is needed. The genetic diversity and population structure of worldwide collections of M. oleifera were investigated using 19 simple sequence repeat (SSR) markers along with a partial sequence of the chloroplast gene atpB which demonstrated large genetic diversity present in wild collections from Pakistan (Shahzad et al. 2013).
Parsimony analyses to infer the phylogenetic relationships of all 13 species of the genus Moringa revealed the four bottle trees in a basal paraphyletic assemblage, with the three species of slender trees, including the economically important M. oleifera forming a clade that is sister to a clade of the six species of tuberous shrubs and trees of northeast Africa (Olson 2002). 20 M. oleifera populations from Nigeria, using amplified fragment length polymorphism (AFLP) primer pairs clustered accessions along eco-geographical lines while others grouped disparately (Popoola et al. 2019).
Model-based population structure of 12 Indian M. oleifera populations using K values from 1 to 20 resulted in five clear populations instead of 12 natural populations. Cluster analysis and structure-based population study showed that no geographical isolation exists between genotypes collected from the southern and northern parts of India (Kumar Ganesan et al. 2014). Population structure analysis of 161 M. oleifera accessions collected from nine other countries of the world was grouped into three clusters and there was a sharp decrease in delta-K values from K2 to K3, with a plateau at K4 (Shahzad et al. 2013). Evolutionary studies of the M. oleifera genome revealed a recent surge of plastid to nucleus gene duplications that led to massive amounts of plastid DNA in the Moringa nuclear genome, representing 4.71%, the largest reported so far (Ojeda-López et al. 2020).
7.9 Conclusion
Moringa oleifera natural populations are broadly distributed throughout Asian tropical and subtropical regions, with rich genetic diversity in their morphology, nutritional and other useful traits. Geographic populations of Moringa species have varied levels of genetic relatedness and distinct genetic parameters. There is a need for concentrated biological, phylogenetic, genomic and biochemical studies on this species. Conservation efforts of Moringa as a genetic resource should be initiated across Asia to prevent extinction. The study of polymorphism and allelic frequencies revealed significantly observed and expected heterozygosity among the sampled populations across the globe, which indicated significant genetic diversity. The combined results of the phylogenetic tree, population structure analysis, and PCA indicated significant clustering across the populations of Moringa oleifera from different regions of the world. However, there is a need for further studies with larger collections to assess genetic diversity and eventually conserve the Moringa populations.
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Lakshmidevamma, T.N. et al. (2021). Genetic Diversity of Moringa (Moringa Oleifera Lam.). In: Boopathi, N.M., Raveendran, M., Kole, C. (eds) The Moringa Genome. Compendium of Plant Genomes. Springer, Cham. https://doi.org/10.1007/978-3-030-80956-0_7
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