Indigenous leafy vegetables of Eastern Africa — A source of extraordinary secondary plant metabolites

Highlights

• Secondary plant metabolites highly vary depending on plant species.

• High concentration of quercetin glycosides in four of five African species.

• Extraordinary hydroxycinnamic acid derivatives occur in amaranth and spiderplant.

• High concentrations of β-carotene, the pro-vitamin A, in amaranth and spiderplant

• Diverse glucosinolate profiles in Brassicales species spiderplant and kale

Abstract

Indigenous African leafy vegetables vary enormously in their secondary plant metabolites whereat genus and the species have a great impact. In African nightshade (Solanum scabrum), spiderplant (Cleome gynandra), amaranth (Amaranthus cruentus), cowpea (Vigna unguiculata), Ethiopian kale (Brassica carinata) and common kale (Brassica oleracea) the specific secondary metabolite profile was elucidated and gained detailed data about carotenoids, chlorophylls, glucosinolates and phenolic compounds all having an appropriate contribution to health beneficial properties of indigenous African leafy vegetables. Exemplarily, various quercetin glycosides such as quercetin-3-rutinoside occur in high concentrations in African nightshade, spiderplant, and amaranth between ~ 1400–3300 μg/g DW. Additionally the extraordinary hydroxycinnamic acid derivatives such as glucaric isomers and isocitric acid isomers are found especially in amaranth (up to ~ 1250 μg/g DW) and spiderplant (up to 120 μg/g DW). Carotenoids concentrations are high in amaranth (up to101.7 μg/g DW) and spiderplants (up to 64.7 μg/g DW) showing high concentrations of β-carotene, the pro-vitamin A. In contrast to the ubiquitous occurring phenolics and carotenoids, glucosinolates are only present in the Brassicales species Ethiopian kale, common kale and spiderplant characterized by diverse glucosinolate profiles. Generally, the consumption of a variety of these indigenous African leafy vegetables can be recommended to contribute to different benefits such as antioxidant activity, increase pro-vitamin A and anticancerogenic compounds in a healthy diet.

Introduction

The African diet comprises of many different ingredients, including leafy vegetables, which contribute to a healthy diet (Baldermann et al., 2016). Apart from playing an important role in the diet, indigenous African leafy vegetables also sponsoring the local economy (Lenne & Ward, 2010), provide environmental services (Frison, 2016b) and are an integral part of African traditional medicine (Padulosi, Thompson, & Rudebjer, 2013). Up to very recently, indigenous African leafy vegetables were regarded in most African communities as food for the poor (Padulosi et al., 2013), despite these advantages. Interestingly, this ideology is rapidly changing. Indigenous leafy vegetables are presently in vogue in some communities in Eastern Africa, and gaining popularity among consumers. In Kenya for example, indigenous African leafy vegetables are sold in large supermarkets in Nairobi, and seed companies are increasingly paying attention towards breeding traditional varieties (Cernansky, 2015). The cultivation area for these vegetables in Kenya increased by 25% between 2011 and 2013 (Cernansky, 2015), also due to increased demand for indigenous African leafy vegetables as people become aware of the benefits of these vegetables. It is therefore common nowadays to find in restaurants, hotels and public canteens, vegetable dishes based on African nightshade (Solanum scabrum), spiderplant (Cleome gynandra), amaranth (Amaranthus cruentus), cowpea (Vigna unguiculata), Ethiopian kale (Brassica carinata) and common kale (Brassica oleracea) cooked solely or in different combinations.

Sub-Saharan Africa with over 10% of the world's population has the highest occurrence of undernutrition in the world (FAO, 2014), with over 70% of rural population who depend mainly on self-produced foods. This situation is typical in Eastern African. Incidences of diet-related diseases like various cancers and cardiovascular diseases are also increasing in these communities (Tullao, 2002). A practical and sustainable option for addressing this multiple burden of malnutrition in such communities is by exploiting the potential of local biodiversity especially with regard to vegetables. The nutritive benefits of a more diversified diet are presently widely recognized (Frison, 2016a). In addition to their richness in minerals and vitamins (Nesamvuni et al., 2001, Yang and Keding, 2009), indigenous African leafy vegetables have been shown to possess anti-oxidative properties and thus have the potential as natural sources for reducing cellular oxidative damage, and suppression of various cancers and cardiovascular diseases (Uusiku, Oelofse, Duodu, Bester, & Faber, 2010). These anti-oxidative properties are due to the presence of a diversity of secondary plant metabolites. However, there is a very limited knowledge on the secondary plant metabolites in indigenous African leafy vegetables and how these contribute to human nutrition and health. Due to the plant species selected flavonoids and hydroxycinnamic acids, carotenoids and chlorophylls are expected in all selected species, whereas and glucosinolates are limited to the Brassicales species.

Flavonoids and hydroxycinnamic acid derivatives are ubiquitous in plants and belong to the group of polyphenols (Mierziak, Kostyn, & Kulma, 2014). The main dietary flavonoids are quercetin and kaempferol present as glycosides in the plant while the main hydroxycinnamic acid is chlorogenic acid. They are of interest due to their antioxidant activity (Zietz et al., 2010), anti-inflammatory and anticancerogenic effects on humans (Chen and Chen, 2013, Pan et al., 2010). Till now, a detailed hydroxycinnamic acid and flavonoid glycoside identification and quantification has not been done in indigenous African leafy vegetables.

In general, all carotenoids have anti-oxidative properties and are associated with a less likely risk of the development of cancer. High uptake of carotenoids is linked to a reduction of cardiovascular diseases (Kopsell & Kopsell, 2006). Some carotenes have pro-vitamin A activity and lutein and zeaxanthin are important eye pigments. High uptake of the latter ones likely reduces the risk of age related eye diseases possibly by protection against oxidative damage. Vitamin A deficiency is the leading cause of preventable blindness in children and increases the risk of disease and death from severe diseases in more than half of all countries, especially in South-East Asia and Africa including Kenya (WHO, 2016). Recently, the WHO estimates that 250 million preschool children are vitamin A deficient and 250,000 to 500,000 vitamin A-deficient children become blind every year (WHO, 2016). Besides supplementation the frequent consumption of pro vitamin A rich vegetables could contribute to improve the vitamin status in rural families. Moreover, a rare number of publications indicate that high uptake of chlorophylls, which co-occur with carotenoids in green leafy vegetables, are associated with reduced risk of certain cancers (Gomaa, Ali, El-Tayeb, & Abdel-kader, 2012). In this context, the indigenous African leafy vegetables could have an important contribution as sources of pro vitamin A, lutein and zeaxanthin as well as chlorophylls.

Moreover, several indigenous African leafy vegetables, such as various cabbage types as well as spiderplant, belong to the order Brassicales which is characterized by a specific group of secondary plant metabolites – the glucosinolates (Verkerk et al., 2009). Glucosinolates themselves are not bio-active, but the evidence was found that some of their corresponding break down product – especially the isothiocyanates – demonstrating anticancerogenic (Lippmann et al., 2014), anti-inflammatory (e.g. Herz et al., 2016) or antidiabetogenic (Guzmán-Pérez et al., 2016, Waterman et al., 2015) properties. Therefore, species containing glucosinolates are of interest for their potential health-promoting effects.

In the context of indigenous African leafy vegetables, there is very little research-based evidence on the profile and richness in these secondary plant metabolites. The present study aims to identify and quantify the plant secondary metabolites in six selected species from Eastern Africa, comprising of five indigenous, and one exotic species (common kale), and focusing on the highly interesting flavonoids and hydroxycinnamic acids, carotenoids, chlorophylls and glucosinolates. Five of the selected vegetables are commonly consumed locally namely African nightshade (S. scabrum), spiderplant (C. gynandra), amaranth (A. cruentus), cowpea (V. unguiculata) and common kale (B oleracea), while the sixth (Ethiopian kale (B. carinata)) is being promoted in urban horticulture across the African continent (Ambrose-Oji, 2009).