Encyclopedia
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Micronutrient malnutrition is a global health challenge affecting almost half of the global population, causing poor physical and mental development of children and a wide range of illnesses. It is most prevalent in young girls, women, and pre-school children who are suffering particularly from the low consumption of vitamins and micronutrients. Given this global challenge, biofortification has proven to be a promising and economical approach to increase the concentration of essential micronutrients in edible portions of staple crops. Produce quality and micronutrient content can be further enhanced with the use of micronutrient fertilizers. Especially developing countries with a high percentage of malnourished populations are attracted to this integrated biofortification, combining modern agronomic interventions and genetic improvement of food crops. Consequently, maize, rice, wheat, beans, pearl millet, sweet potato, and cassava have all been biofortified with increased concentrations of Fe, Zn, or provitamin A in various developing countries. Today, there are several large-scale success stories in Africa and Asia that support the research and development of biofortified crops.
- micronutrients
- developing countries
- agronomic biofortification
- genetic biofortification
- malnutrition
- hidden hunger
1. Introduction
Mineral micronutrient deficiencies in humans are widespread globally, especially among women and children. Micronutrients are needed in the human diet in minute quantities, yet it is estimated that over 3 billion people suffer from micronutrient deficiencies, resulting in deleterious impacts on human health [1][2][3][4][5]. The prevalence and devastating impacts of micronutrient deficiencies are exacerbated in areas where cereal grains constitute a large portion of the diet, dietary diversity is low, and/or supplementation/fortification programs are lacking [1][2]. Micronutrient deficiencies impair growth, cognitive development, and immune function, with often lifelong consequences [6]. Therefore, this ‘hidden hunger’ poses many burdens on human health, economic growth, and constrains efforts to alleviate poverty. With a continuously growing population and changing diets, food demand is increasing drastically but the space for agriculture is limited leading to intensive use of natural resources and often poor-quality agricultural produce. Agricultural interventions to enhance the nutritional value of edible and forage crops feeding livestock could help to improve human nutrition, especially in developing countries.
One option to reduce micronutrient deficiencies is biofortification, defined as the process of improving the nutritional value of edible crops through selective conventional breeding, mineral fertilization, or advanced transgenic approaches. Additionally, the quality of the produce, post-harvest losses, food taste, cooking time, yield, and pest resistance can also be improved along with the biofortification process. Biofortification targets concentrate mostly on people living in rural areas depending mostly on their staple crops to fulfil their food requirements. Biofortified crops may make their way into local retail outlets and as a result, particularly people in rural areas could be reached comfortably. Their diets consist mostly of staple foods, and they are hard to reach through other strategies of nutritional improvement (e.g., fortification of processed food or supplements). Therefore, the lack of nutrients in the food they consume daily can at least be minimized if not eliminated entirely [7]. Although populations in urban areas may have some access to commercially fortified and processed foods, biofortified staples may still be more beneficial to them, especially for poor people who have limited access to expensive fortified and diversified food.
Biofortification offers many advantages for developing countries by using various strategies including engineering of staple crops [8]. As the World Health Organization considers iron (Fe), zinc (Zn), and vitamin A as the most limited micronutrients, research and programs such as HarvestPlus are focusing on these micronutrients to improve the most common crops such as corn, wheat, and rice [6]. These common crops are available for everyone globally and do not need special management, because the enrichment of produce can be achieved without affecting the crop’s productivity. As most of the target minerals are also important for the plant’s own nutritional requirements and may contribute to environmental stress tolerance, it can even result in better growth and higher yields. This is particularly important when the environmental conditions for farming are inferior, as they often are in developing countries, and the new varieties have an advantage over conventional varieties [8].
It is the general target in all breeding efforts for biofortification to reach or even improve the yield level of non-fortified varieties. Despite the complex breeding process, most biofortified crops have been developed and mapped using conventional breeding, and transgenic approaches were used in a few cases only [6]. For example, conventional breeding led to the development of rice with enhanced Zn and Se content [9], wheat with higher grain Fe and Zn [10], or maize enriched with provitamin A [11]. A common example of a genetically biofortified crop is golden rice, which consequently has faced a lot of criticism due to various social and political concerns. The issue of genetically modified crops is still under debate in most developed countries, nevertheless, developing countries discuss the potential of genetically modified nutrient-enriched crops because of the large number of poor people prone to micronutrient malnutrition.
A big challenge of biofortified food crops is acceptance by the consumers, which determines the demand for the crop to be cultivated by farmers [11]. For example, the color difference between the ordinary and a biofortified crop with higher concentration of β-carotene demands considerable efforts to generate its market. In Africa, where common corn for human consumption is white and the yellow one is for animals, consumers need to be convinced to buy yellow corn for human use [8]. If the crops have the same color, consumers must be able to distinguish the ordinary crop and the one enriched with nutrients. Both problems must be solved with information and communication between scientists, farmers, and consumers until the biofortified food is accepted and well known [8]. However, even then, the transport to remote markets may be difficult and indigenous markets need to be developed [8].
2. Biofortification of Cereals
Increases of a few milligrams of essential minerals’ concentrations in staple cereals can affect millions of people around the world by making their life healthy and more productive. Significant health, social, and economic benefits can be achieved by biofortification of cereal crops which can provide an increased supply of minerals to plants and ultimately to consumers.
2.1. Wheat
Wheat grain makes a major contribution to the human diet as it provides many nutrients and minerals. Therefore, wheat production is required to double by 2050 for global food security [12]. Wheat germplasm has been extensively screened for its mineral contents of Fe, Zn, Se, Mn, Mg [13][14][15][16][17], proteins [18][19], and vitamins [20]. The screening also included phytic acid which is important due to its role in limiting the bioavailability of nutrients [21][22][23]. Breeding as well as agronomic and genetic solutions have been dissected for the objective of wheat biofortification in recent decades. The dedication of the International Maize and Wheat Improvement Center (CIMMYT) gene bank and the Harvest Plus project set the basis by breeding competitive bread wheat cultivars with 40% higher Zn concentration in South Asia [24][25][26]. Following this process, five biofortified wheat cultivars have been released, cv. Zincol 2016 in Pakistan, cv. Bari Gom 33 in Bangladesh and cv. Zinc Shakti (Chitra), WB02 and HPBW-01 in India. Ranges of Fe concentrations of 20–60 mg kg−1 and Zn concentrations from 15 to 35 mg kg−1 in a set of high yielding genotypes were reported [15]. This confirmed that sufficient genetic variation exists within the wheat gene pool that can be explored for substantial increases in grain micronutrient concentrations. In addition, up to 3-fold enhancements of Fe and Zn concentrations in wheat grains through soil and foliar application methods have been reported [13][27]. Creating awareness for balanced fertilization among farmers in the developing world will further contribute to meet micronutrient concentration targets to combat hidden hunger. Enhancing the concentration of Zn and Fe in the most edible part, the endosperm, is not simple to achieve through agronomic practices, nevertheless, an increase in concentration of Fe and Zn through soil application has been reported [28][29][30].
2.2. Rice
Rice is particularly highlighted for micronutrient improvement due to its global role as one of the main staple food crops, giving rice biofortification a huge potential for alleviation of malnutrition globally. In 2013, the first high Zn rice cultivar (with 20–22 mg kg−1 Zn in brown rice) was spread through Harvest Plus and the Bangladesh Rice Research Institute. Increases of 17.4, 0.123, and 14.2 mg kg−1 for Zn, Se, and Fe, respectively, have been reported in rice by [31]. Provitamin A biofortified “Golden Rice” has proved itself as a cost-effective intervention in the areas where rice is the staple crop [32]. Recently, [33] screened 484 rice lines and found co-localized QTL regions for Fe and Zn along with high yield attributes. The composition of rice grains, including localization of Fe and Zn, their chelators, transporters, promoters, and inhibitors, needs to be considered in order to improve the bioavailability of micronutrients in rice and consequently the nutrition and health of consumers [33]. Zinc management in soil has also significantly improved the grain Zn content in aromatic rice [34][35].
2.3. Maize
Maize is often considered a cash crop, but it is also a staple in many countries and provides food for humans and animals globally. Exogenous application of Zn in the form of seed priming, foliar spray, or incorporated in the soil enhance the germination of maize seed, seedling vigor, and tolerance against different stresses [36][37]. Maqbool and Bashir [38] reported high accumulation of Zn, i.e., 36 mg kg−1, in maize grains with application of ZnO nano-particulates. Significant genome-wide association between micronutrient concentration in maize kernel and yield has been reported previously, suggesting that biofortification of maize is achievable using specialized phenotyping tools and conventional plant breeding techniques [39][40][41]. Among 1000 CIMMYT maize lines, concentration ranges of Zn, Fe, and provitamin A have been reported, and maize lines with 15–35 mg kg−1 Zn, an average of 20 mg kg−1 Fe, and about 0–15 mg kg−1 total provitamin A concentration have been identified [42].
2.4. Pearl Millet
Pearl millet (Pennisetum glaucum L., R. Br.) is a major warm-season cereal grown in the arid and semi-arid tropical regions of Asia and Africa and is used as food and fodder. It is a staple food for millions of people in Africa and Asia and contains higher levels of micronutrients such as Zn and Fe than wheat and rice. Variation in Fe concentration (35–116 mg kg−1), Zn (21–80 mg kg−1), and protein (6–18%) were reported in 281 advanced breeding lines bred at ICRISAT by [43]. Pearl millet has also been shown to exhibit great genetic variation (30–140 mg kg−1 Fe and 20–90 mg kg−1 Zn) which can be used to breed new cultivars that have high contents of Zn and Fe and are high yielding. Pujar et al. [43] found highly significant and positive correlations between general performance and Fe/Zn density in pearl millet populations. Incorporation of parental lines with a high degree of average heterosis could prove to be beneficial in breeding programs with a focus to enhance Fe/Zn in pearl millet [44]. The high iron and zinc pearl millet varieties AIMP92901 and ICMR312 have been developed by [42]. In India, open pollinated pearl millet varieties (Dhanashakti) and hybrids (ICMH 1202, ICMH 1203, and ICMH 1301) with high concentrations of iron (70–75 mg kg−1) and zinc (35–40 mg kg−1) have been introduced [45][46].
3. Biofortification of Non-Cereals
There are a number of non-cereal crops that are contributing to food security worldwide, especially in many African countries. Both agronomic and genetic biofortification are applicable for non-cereals as well. Few of them have been mentioned yet, nevertheless, biofortification of other crops such as pulses also has significant potential such as biofortification of chickpea [47].
3.1. Cassava
In many African countries, cassava (Manihot esculenta) is a staple, but it contains only low concentrations of Zn, Fe, I, and vitamin A. Therefore, there is a need to biofortify this crop for Fe, Zn, I, and vitamin A in poor resource countries to reduce micronutrient deficiencies. Outside of Africa, cassava is also used as a staple crop in Latin America and Caribbean countries. It is being considered an important crop to biofortify with beta carotene to enhance the vitamin A level of its consumers [48]. Cassava is tolerant to various stresses and poor soils, therefore, an important crop for tropical and sub-tropical climatic conditions.
Ortiz-Monasterio et al. [49] investigated and introduced transgenic cassava that can accumulate a high concentration of beta carotene in roots based on nptII, crtB, and DXS genes. It has been described that transgenic cassava is high in concentration of carotenoid through overexpressing a PSY transgene [50]. However, the natural variability of carotene contents in cassava is also high and linked to the color of roots. It is reported that higher carotene content is observed in orange varieties (12.6 µg g−1) while low carotene content is found in white varieties (1.3 µg g−1).
In African countries, cassava has been utilized for mitigation of beta carotene deficiency by the partnership of Harvest plus with the International Institute of Tropical Agriculture (IITA), and they are utilizing beta-carotene biofortified cassava for mitigation of vitamin A deficiency in rural populations. Until 2014, this partnership has produced six vitamin A fortified varieties of cassava in Nigeria, i.e., TMS 01/1368-UMUCASS 36 and TMS 01/1412-UMUCASS 37 in2011, TMS 01/1371-UMUCASS 38, NR 07/0220-UMUCASS 44, TMS 07/0593-UMUCASS 45, and TMS 07/539-UMUCASS 46. Meanwhile, biofortified cassava has been introduced in many more countries. Cassava also has a wide variety of genotype modifications for minerals (Fe and Zn) and proteins that resulted in the development of enhanced nutritional standards for cassava [51] and this diversity is a potential asset for the development of Fe, Zn, and protein enriched cassava varieties.
3.2. Potato
Potato (Solanum tuberosum) is an important vegetable and a good source of energy and calories for people of all ages. As it is being used globally, it has great potential to improve human nutrition through various biofortification strategies. Using transgenic techniques, the beta-carotene contents of potato have been enhanced by adding the PSY gene [52].
Field experiments were conducted to enhance Zn content in potato tubers by foliar application of Zn fertilizers which increased tuber Zn content significantly. It was also observed that zinc sulfate and zinc oxide were more productive than zinc nitrate for foliar applications targeted at enhanced Zn concentrations and improved yield [53].
Similarly, it was shown that the selenium (Se) concentration in potato tubers was enhanced by foliar application of selenite and selenate [54]. The Se content of potato tuber also improved by foliar application of Se with humic acid [55]. In addition, potato is also a good source of antioxidants for human health. Additionally, the contribution of potatoes as a source of antioxidants and nutritive properties was related to the natural variation of red and purple pigments in cultivated potato germplasm. Thus, breeders are paying serious attention to the breeding of these variants [56]. In summary, potatoes have considerable genetic diversity for micronutrient concentration that can be utilized for conventional breeding of varieties with enhanced Fe and Zn concentrations for human nutrition [57].
3.3. Sweet Potato
Orange-fleshed sweet potato (Ipomea batatas L., Lam) varieties have a higher beta carotene content than white fleshed varieties. The main objective of the sweet potato biofortification initiative is replacing white fleshed varieties with orange fleshed plants. The target level of beta carotene set by the Harvest Plus project for sweet potato is 32 mg kg−1 but cultivars with higher concentrations of up to 100 mg kg−1 have been reported by HarvestPlus [49] and Nestel et al. [58]. In addition to the value of sweet potato as an essential source of natural antioxidants and bioenergy, it is also enriched with several phytochemicals, vitamin C, carbohydrates, anthocyanin, and dietary fiber [59]
The nutritive value of sweet potato can be improved by enhancing the contents of lutein, carotene, and total carotenoids, through overexpression of “orange” IbOr-Ins genes in white fleshed sweet potato [60]. The orange fleshed sweet potato beta carotene content can also be enhanced by irrigation and chemical fertilizer applications [61].
To overcome malnutrition issues, developing countries grow about 95% of the global sweet potato crops, with a major portion being grown in China. Therefore, sweet potato was selected for the amelioration of vitamin A deficiency. Harvest Plus and the International Potato Centre have improved various cultivars of orange sweet potato through high vitamin A content. Six varieties of the sweet potato were released in Uganda, i.e., Ejumula, Kakamega, Vita, Kabode, Naspot 12O, and Naspot 13O, and three in Zambia, i.e., Twatasha, Kokota, and Chiwoko. The orange sweet potato developed by Harvest Plus has already shown a remarkable impact on nutrition and food security in Africa, which was acknowledged with the World Food Prize, 2016.
3.4. Common Beans
The common bean (Phaseolus vulgaris) is an essential grain legume, consumed by humans in all parts of the world. It is an annual herbaceous plant and its dry grains are edible. The beans are a rich source of amino acids, i.e., threonine, valine, leucine, isoleucine, and lysine, but its nutritive value is insufficient due to low concentrations of the essential amino acids methionine and cysteine. However, the methionine concentration in beans can be enhanced through expression of methionine-rich storage albumin protein from seeds of the Brazil nut [62].
Common beans also have a potential for Zn biofortification through foliar application of Zn fertilizer [63][64]. It has been reported that in common beans N, P, K, Mn, Cu, and Zn concentrations can be enhanced by the administration of organic and chemical fertilizers [65]. Furthermore, it has been shown that in common beans the Fe concentration can be enhanced by 60–80% and Zn concentration by around 50%, using different strategies. High genetic diversity in common beans has been discovered for Fe and Zn concentration [66][67] and genes have been reported in navy bean that are related to Zn accumulation [68]. Generally, staple crops are poor sources of dietary folates but legumes and particularly beans were shown to be a good source of dietary folates [69].
Thus, biofortification of common beans with minerals and amino acids can play a significant role to uplift the nutritional status of resource poor people of developing countries and promising work is in progress.
4. Effectiveness of Biofortification and the Way Forward
Considering current developments and future predictions, mineral and vitamin deficiencies are expected to be more threatening across the globe, but especially in developing countries, due to fast growing populations, resource limitations, decline in natural resources, lack of awareness, and social behaviors. Balanced diets and/or provision of limiting nutrients including minerals, vitamins, and protein is crucial to keep upcoming generations healthy. Due to lack of education and economic deteriorations in many developing countries, it will be very difficult to accomplish the target of zero hunger declared in the United Nations Sustainable Development Goals (SDGs). However, the significant progress made by biofortification during the last two decades provides hope for developing countries to combat their nutritional issues. Biofortification is a low-cost crop-based approach holding great promise to achieve the targets of healthy nutrition in the developing world. As described, significant impact has been achieved and future strategic research and appropriate policy could lead to great success in biofortification in upcoming years.
Crop biofortification offers the economic, easily accessible, and scalable solution for improved crop varieties with nutritionally dense grains. A great resource of exploitable genetic variation has been documented across gene pools in a wide range of crops. The accelerated selection or incorporation of gene(s) that enhance the nutrient content in staple crops will largely determine the success of various nutritional breeding schemes. Collaborative research efforts involving breeders, biotechnologists, physiologists, biochemists and, importantly, nutritionists are needed to strengthen biofortification programs to meet the challenge of attaining global nutritional security.
The biofortified cropping system is highly sustainable as nutritionally improved varieties will continue to be grown and consumed year after year, even if government attention and international funding for micronutrient issues fade. Combined with the use of mineral fertilizers, such systems can enhance the mineral content in cereals, vegetables, and fruits durably in a very cost-effective way without the need for costly centralized programs. The staple crops enriched through fertilizer applications in soils or on foliage can be as effective as varieties developed by breeding or genetic engineering although the combination of both technologies is probably the best approach. Moreover, biofortification provides a truly feasible means of reaching malnourished populations in relatively remote rural areas, delivering naturally fortified food to people with limited access to commercially marketed fortified foods, which are more readily available in urban areas. Thus, there is a strong case to spend more resources to promote and augment strategic research on biofortification sustaining the available resources and exploiting the available potential wisely and sustainably. It complements work for higher yielding cropping systems, the conservation of soil fertility and improvement of soil health by sustaining and improving soil organic matter, effective application of fertilizers and development of nutrient enriched staple crops using conventional breeding and, where necessary, transgenic approaches.
However, the impact of biofortification will also depend on the development of sustainable markets for biofortified seeds and products. Post-harvest handling, storage losses of biofortified nutrients, and market segregation of biofortified crops are research topics that still need more attention. Seed producers must have access to biofortified varieties and be made aware of the market opportunity. Consumers need to receive information on the nutritional benefits of biofortified crops as well as their characteristics to actively choose biofortified crops over comparable non-biofortified varieties. Further on, biofortified products need to be advocated to food processing companies to mainstream biofortified crops beyond small rural markets. Behavior change communication and effective promotional efforts are therefore essential to achieve acceptance by farmers, consumers, policy makers, and other stakeholders. We conclude that for many “new” biofortified varieties, there is still need for context-specific, innovative solutions to achieve widespread adoption.
