Avnee
Sonia Sood2- 1Department of Agronomy, CSK Himachal Pradesh Krishi Vishvavidyalaya, Palampur, India
- 2Department of Vegetable Science and Floriculture, CSK Himachal Pradesh Krishi Vishvavidyalaya, Palampur, India
Micronutrient deficiency also known as “hidden hunger” refers to a condition that occurs when the body lacks essential vitamins and minerals that are required in small amounts for proper growth, development and overall health. These deficiencies are particularly common in developing countries, where a lack of access to a varied and nutritious diet makes it difficult for people to get the micronutrients they need. Micronutrient supplementation has been a topic of interest, especially during the Covid-19 pandemic, due to its potential role in supporting immune function and overall health. Iron (Fe), zinc (Zn), iodine (I), and selenium (Se) deficiency in humans are significant food-related issues worldwide. Biofortification is a sustainable strategy that has been developed to address micronutrient deficiencies by increasing the levels of essential vitamins and minerals in staple crops that are widely consumed by people in affected communities. There are a number of agricultural techniques for biofortification, including selective breeding of crops to have higher levels of specific nutrients, agronomic approach using fertilizers and other inputs to increase nutrient uptake by crops and transgenic approach. The agronomic approach offers a temporary but speedy solution while the genetic approach (breeding and transgenic) is the long-term solution but requires time to develop a nutrient-rich variety.
Introduction
Over 2 billion people worldwide suffer from micronutrient deficiency which has a negative impact on their health and socio-economic condition (1). The principal reason is the consumption of cereal-based food which provide enough calories but they are deficient in phytochemicals (minerals, vitamins, antioxidants, and fiber). These phytochemicals are essential for the normal growth and development of humans and their deficiencies can have serious health consequences, including diminished cognitive degeneration in children, increased risk of infections and a range of other negative effects on physical and mental health.
Green Revolution, which took place from the mid-20th century onwards, marked a significant shift in agricultural practices and policies, particularly in developing countries like India. During the revolution, the emphasis was shifted on boosting crop productivity, notably that of rice and wheat, which led to the domination of these two crops in the nation. The increased productivity ensured food security in the country but on the other hand, decreased bio-diversity resulted in a monotonous cereal-based diet and thus increased concern about nutritional security. The ever-growing population of India further worsens the problem of providing sufficient nutrients to all. Over 21.9% of the Indian population is living in extreme poverty with limited access to resources (2). With their poor purchasing power, they consume what they produce in their fields. In order to alleviate malnutrition and to attain nutritional security in the country, a second green revolution is therefore required, with a particular emphasis on the development of biofortified, nutrient-rich varieties.
Staple crops, such as rice, wheat and maize are the main source of calories for a large proportion of the world’s population, particularly in low-income countries. These crops, however, often lack essential vitamins and minerals, which might result in micronutrient deficiency. Biofortification can help to address this problem more sustainably and economically by increasing the levels of essential vitamins and minerals in staple crops. It is the process of enrichment of bio-available concentration in edible portions of food and aims at providing nutrient-rich food to rural resource-poor people who do not have access to diversified food, supplements and industrially fortified food (see Figure 1). Biofortification can be a cost-effective and sustainable way to address micronutrient malnutrition at the population level with an ultimate goal to reduce malnutrition and improve public health, particularly in populations that rely heavily on a single staple crop for their daily caloric intake. It requires a one-time investment unlike supplements, reach malnourished poor population and provide better quality food without compromising yield (see Figure 2). This can be particularly important in developing countries where micronutrient deficiencies are common and can have serious health consequences. Iron, zinc, iodine and selenium deficiencies are the most common, which account for around 60% of iron, 30% of zinc and iodine and 15% of selenium deficiency (3). However, biofortification alone is not enough to eradicate malnutrition. It cannot provide such a high level of nutrients as through supplements or fortified food but they improve daily dietary intake of nutrients (4). In the context of climate change also, the anticipated drop in dietary micronutrients makes biofortification more important for vulnerable groups to maintain good health.
Figure 1. Different countries and their percentage of population suffering from malnutrition.
The concept of simultaneously biofortifying crops with multiple essential micronutrients is an innovative and promising strategy to address widespread nutrient deficiencies and improve overall human nutrition. This approach, often referred to as “multi-nutrient biofortification” or “combinatorial biofortification,” aims to create crops that contain a balanced array of various essential vitamins and minerals. This strategy can provide a more holistic and comprehensive approach to combating malnutrition by addressing multiple nutrient deficiencies concurrently. By combining different nutrients in crops, their overall bioavailability and health benefits can be maximized. Multi-nutrient biofortified crops can encourage dietary diversity as people consume a wider range of nutrients from staple foods. In addition to cost savings from development to distribution and synergies through aggregated health effects, multi-nutrient biofortification can result in significantly higher market coverage by preventing competition between numerous single-nutrient biofortified varieties (5).
Approaches of biofortification
Figure 2. Methods of biofortification (Agronomic, Breeding and Transgenic).
Agronomic biofortification
Agronomic biofortification refers to the process of enriching the nutritional value of crops through fertilization and soil management. It offers an efficient and timely solution that is the quickest and most affordable way to produce nutrient-dense food, albeit it only offers a short-term fix. The majority of crops can benefit from this very simple method of biofortifying with iron, zinc, iodine, and selenium. To boost the content of micronutrients in the plant’s edible parts, micronutrient-containing organic/inorganic fertilizers or biofertilizers are applied to the plant by foliar or soil application. Micronutrient concentration depends on the source of fertilizer used, method and rate of fertilizer application, stage of application, and translocation of nutrients within plants. Due to variations in mineral mobility, mineral accumulation among plant species and soil compositions in the particular geographic region of each crop, the success of agronomical biofortification is highly variable (6). The effectiveness of agronomic biofortification has increased with the development of high specialized fertilizers with high nutrient uptake efficiency and greater nutrient translocation to the consumable sections of a crop plant, which include water-soluble fertilizers, chelated fertilizers and nano-fertilizers (7).
Nanoparticles, which are extremely small particles with unique properties due to their size and structure, have gained attention as potential tools for biofortification. Nanofertilizers (NFs), a subset of nanotechnology applications in agriculture, hold significant potential to revolutionize traditional methods of enhancing crop nutrient content and improving overall nutritional quality. By harnessing the unique properties of nanoparticles, NFs offer a promising avenue for increasing the concentration and bioavailability of essential nutrients in food crops, a strategy known as “nanofertilizer-assisted biofortification.” Because of the large increase in surface area and the NFs’ small size, plants can easily absorb the particles (8).
Iron biofortification
Iron deficiency is a common problem, particularly in developing countries and it can have serious health consequences such as anemia affecting over half the population of children under the age of five and pregnant women in India. Biofortification can help to address this issue by increasing the iron content of crops, which can in turn help to improve the iron intake of individuals who rely on these crops as a dietary staple. Iron is a vital nutrient for humans, it is required for proper body functioning but cannot be produced by the body and must be obtained from the diet. It is crucial for the production of red blood cells and the transportation of oxygen within the human body, supporting the immune system, providing energy and maintaining healthy skin, hair and nails. It is especially important for pregnant women, infants, and young children, as they have higher iron requirements. Anemia, weariness, and immune system impairment are just a few of the health issues that iron deficiency can cause, especially in impoverished nations where plant-based foods are the main source of Fe (9).
Applying iron-rich fertilizers to the soil and proper soil management, such as maintaining the pH and nutrient balance of the soil can help to improve the uptake of iron by crops. It is important to note that the efficacy of these methods can vary based on the particular crop and growing circumstances. Comparing vegans to meat-eaters, the former should consume 1.8 times more of the recommended daily intake (RDA) of Iron than later (10). Table 1 shows some of the crops that are successfully agronomically biofortified with iron.
Table 1. Agronomic biofortification of iron.
Zinc biofortification
Zinc is a crucial micronutrient that is necessary for both plants and humans. It is involved in a wide range of physiological functions including immune response, protein and DNA synthesis, wound healing and involved in the metabolism of carbohydrates, proteins and fats. Zinc deficiency is a major public health problem affecting around 30% of the world’s population, making people more susceptible to issues including maternal mortality, DNA damage, growth retardation, changes in taste and smell, immunological dysfunction, and an increased risk of infections (23).
Biofortification can assist to solve the issue of zinc deficiency and improve the nutritional value of crops, particularly in areas where deficiency is prevalent. Zinc deficiency in humans and soil show geographical overlap (24). A high percentage of agricultural land (36.5%) in India is zinc deficient and cultivating crops on these deficient soils further reduces zinc levels in edible portions (25). The deficit is particularly prevalent in low-income developing nations where a plant-based diet is the norm (26). Agronomic biofortification of zinc was reported to be successful in a large number of crops (Table 2).
Table 2. Agronomic biofortification of zinc.
Iodine biofortification
Iodine is a necessary component of human metabolism and crucial for the proper function of the thyroid gland in humans, energy production and body temperature regulation, despite not being a necessary element for plants, although its application has been linked to higher yields and high iodine content in several crops (Table 3). It is estimated that the iodine intake of 30–38% of people worldwide is insufficient (45).
Table 3. Agronomic biofortification of iodine.
Iodine deficiency can lead to a variety of health problems, including goiter, infertility, growth impairment, hypothyroidism and intellectual disability. Iodine biofortification can be a particularly useful approach in areas where iodine deficiency is common and people rely heavily on plant-based foods as a source of nutrients. Biofortified plant-based foods can help to increase the overall iodine intake of a population and improve the nutritional status of individuals who consume these foods. Adults should consume between 150 to 290 μg of iodine per day, with a tolerable upper limit of 1,100 μg per day (53, 54). One of the most common ways to fortify iodine is through the addition of iodine to salt. This is called iodized salt. Iodized salt may not be effective in preventing iodine deficiency in all populations as it can raise blood pressure which is a major risk factor for heart disease and stroke. It is also linked to an increase in cases of osteoporosis, a condition that causes the bones to become weak and brittle. A promising strategy to raise the iodine content of crops is agronomic biofortification.
Selenium biofortification
Selenium is a trace element that is essential for human health. Due to its incorporation into selenoproteins like glutathione peroxidase, which perform a number of functions including antioxidant activity, it is essential for the immune system’s proper operation (55). Se deficiency affects hundreds of millions of people around the world (56). For plants, Se is not essential (57, 58), but when applied at low doses, it is beneficial for some groups of plants by increasing the activity of various enzyme systems; selenium alone or in combination with iodine was found to increase concentration, better quality in some plants (Table 4); for example, it delays tomato fruit ripening by inhibiting ethylene biosynthesis and enhancing the antioxidant defense system (80).
Table 4. Agronomic biofortification of selenium.
Plants can absorb selenium from the soil, but the availability of selenium in the soil can vary widely. In some areas, the soil may be naturally low in selenium, while in others, selenium may be present but not in a form that plants can easily absorb. To ensure that plants are getting sufficient selenium, it may be necessary to add selenium to the soil. This can be done through the use of selenium fertilizers or through the application of selenium-rich compost or manure. It is also possible to provide selenium to plants through the use of selenium-rich irrigation water or through the use of selenium-enriched seeds.
Interaction among nutrients
The effectiveness of agronomic biofortification can be affected by interactions between macronutrients and micronutrients (81) (see Table 5). While previous biofortification initiatives have mainly concentrated on increasing specific nutrients, a novel strategy could be to simultaneously biofortify crops with a number of essential micronutrients, providing a more comprehensive nutritional profile. Some nutrients work synergistically in the body, enhancing the absorption and utilization of others. Zinc, for example, improves nitrogen metabolism by promoting effective uptake and assimilation. It also aids in the conversion of phosphorus into forms that are easily absorbed by plants, as well as in the regulation of stomatal function and water movement, both of which affect potassium absorption. The synthesis of selenium-containing phytochemicals, such as selenocompounds can be improved by selenium biofortification. According to (82, 83), plants convert selenium into selenoamino acids, which are then converted into phytochemicals. These substances have antioxidant qualities beneficial to human health. Selenium also plays a role in reducing element toxicity and regulating the concentration of micronutrients in plants by modifying soil conditions, encouraging microbial activity, taking part in crucial physiological and metabolic processes, generating element competition, stimulating metal chelation, organelle compartmentalization and sequestration (84). It is preferable to combine Zn, Se, and Fe in conjunction with the employment of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungus (AMF), in order to develop biofertilizers that are ecologically benign yet result in crops that are enriched in microelements (85).
Table 5. Effect of nutrients on other nutrients and phytochemicals.
In some cases, certain nutrients can compete with each other for absorption. By ensuring an adequate balance of multiple nutrients, competition for absorption can be minimized. Adequate levels of nutrients like magnesium, zinc and manganese are important for vitamin C synthesis. These nutrients can impact the enzyme systems involved in ascorbic acid production. Certain micronutrients, such as copper and manganese, are cofactors for enzymes involved in the synthesis of antioxidants and flavonoids (86). Adequate levels of these micronutrients can positively influence the production of these compounds. The formation of roots, the movement of shoots and the re-localization of nutrients from vegetative tissue to the seeds are all positively impacted by a plant’s N and P status. As a result, the crop’s edible sections absorb more micronutrients and have higher concentrations of them (87).
Salt, high/low temperature, heavy metals, and drought all cause the overproduction of reactive oxygen species (ROS) and the induction of oxidative stress in plants (85). It has been demonstrated that biofortification with Zn, Se, and Fe using various types and forms of fertilizer can reduce the damage caused by oxidative stress by increasing the content of ROS-scavenging enzymes such as superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), glutathione peroxidase (GPX), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), glutathione reductase (GR), glutathione S-transferase (GST), and peroxiredoxin (PRX) content in different sites of plant cells (88, 89).
Biofortification through conventional breeding
Traditional plant breeding is a method of improving the nutritional content of crops by selecting for desired traits through controlled crosses between different plant varieties. The process involves selecting plants with desirable traits, such as higher micronutrient content and crossing them with other plants to create a hybrid with improved characteristics. Over time, this process is repeated and the offspring are screened for desired traits.
Plant breeding techniques are used in the biofortification approach to develop staple food crops with greater micronutrient content (97), this assists to target low-income households in the country. Numerous crops have been targeted for biofortification through crop breeding due to their improved acceptance (Table 6). A biofortified crop system is highly sustainable. Nutritionally improved varieties will continue to be grown and consumed year after year, even if government attention and international funding for micronutrient issues fade (105). Since the last four decades, yield qualities and resistance breeding have received the majority of attention resulting in lower amounts of nutrients in the existing varieties (106).
Table 6. Varieties developed through conventional breeding.
Biofortification by breeding is attained when crops have naturally some concentrations of micronutrients, such as iron, zinc and vitamin A, which means when genetic diversity is accessible in usable form. Some examples of biofortified crops include iron-rich beans, zinc-rich rice, selenium-rich rice, wheat and maize, iodine-rich cassava, maize, and sweet potatoes and vitamin A-rich sweet potatoes.
This method is widely accepted as it is safe and does not raise the same safety concerns as genetic engineering. However, traditional breeding can be a slow and labor-intensive process, and it may take many years to develop a crop with improved nutrient content.
Target crops for biofortification
Cereals
Rice, wheat and maize are the major calorie supplement for two-thirds of the Indian population thereby ruling the people’s diet in the country. Biofortification of cereals with iron, zinc, protein and provitamin-A content can assist to bring down the issue of hidden hunger in the population who does not have access to diversified food or supplements. Cereals are typically deficient in both protein and vitamin A. Proteins are vital for humans as they build cells, act as enzymes for chemical reactions, regulate hormones, support the immune system, aid in muscle function, and facilitate communication between cells, among other essential roles in maintaining overall health and bodily functions. Dietary protein deficiency can lead to varied effects on body weight and composition. Inadequate protein intake often results in increased food consumption, body weight, and fat mass. Extremely low protein diets cause fatty liver, reduced energy absorption, and persistent decreases in lean mass (107). Vitamin A aids in cell communication, supports reproduction and growth, and acts as an antioxidant to protect cells. Its deficiency can cause problems in the eyes (ophthalmological), skin (dermatological), and immune system (immune impairment) (108).
Polished rice is a poor source of micronutrients; 60–80% of Fe and around 30% of Zn are lost during polishing (109) yet consumers prefer polished rice because of their long storage and their taste preference. Pureline varieties of rice developed by ICAR-IIRR are DRR Dhan 45, DRR Dhan 48 and DRR Dhan 49 having zinc content ranging from 22.6–25.2 ppm. Protein-rich variety CR Dhan 310 has 10.6% protein content in polished rice in comparison to 7.0–8.0% in popular varieties.
Wheat is the second main crop of India after rice. Breeding wheat to improve the quality of the crop has become the recent focus. However, farmers’ acceptance of nutrient-dense cultivars and the introduction of new biofortified varieties into wheat-growing areas is crucial in the fight against hidden hunger (110, 111). Although iron and zinc are abundantly present in the aleurone layer, however, their bioavailability is affected by the presence of phytate (112).
Supplementing with vitamin A presents a problem due to its high cost and need for efficient transportation and storage methods, which are challenging to implement in remote, sparsely populated locations (113). Maize is an ideal crop for biofortifying it with provitamin A due to its natural diversity in carotenoid content, which includes predominant carotenoid components lutein and zeaxanthin, as well as β & α-carotene and β-cryptoxanthin (114). Traditional maize contains less amount of proteins, lysine and tryptophan, over-dependency on this cereal causes diseases such as kwashiorkor and pellagra (115, 116). There are presently several varieties of quality protein maize (QPM) being grown throughout the country having high lysine and tryptophan levels.
Pulses
Pulses are a major source of protein and other vital nutrients for millions of people, especially in developing countries. Biofortification can effectively address malnutrition by providing more of the key nutrients needed for proper growth, development and overall health. Pulses are not only nutritionally valuable but also environmentally beneficial, as they have the ability to fix nitrogen in the soil, enhancing its fertility. Lentils and beans are particularly promising candidates for enhancing iron and zinc content through conventional breeding methods. These pulses exhibit inherent genetic potential for heightened mineral accumulation. Harnessing this natural richness entails meticulous selection of parental genotypes demonstrating superior mineral concentrations. Through systematic interbreeding over successive generations, novel cultivars can be developed wherein augmented iron and zinc levels are seamlessly integrated while preserving key agronomic attributes. Consequently, these biofortified varieties emerge as pivotal assets for ameliorating micronutrient deficiencies and fostering enhanced nutritional quality within food systems.
Vegetables and fruits
The consumption of vegetables and fruits is important for a healthy diet, as they are rich in vitamins, minerals, fiber, and other essential nutrients. They offer a diverse, low-calorie, protective and nutrient-dense diet. It has long been understood that eating the recommended amounts of vegetables and fruits has favorable health effects and frequent consumption of a range of these foods has been associated with decreased risk of diseases. The benefits of biofortifying vegetables and fruits include reducing the risk of chronic diseases, increasing economic productivity and promoting overall health and well-being.
Biofortification through transgenic/biotechnological means
Biotechnology is a field of science that uses living organisms, cells or their components to make useful products or services. It has the potential to solve many of the world’s most pressing problems, such as producing enough food to feed a growing population, developing new treatments for diseases and enhancing the nutritional quality of crops. Biotechnology allows more precise and efficient targeting of specific nutrients than other means.
Nutritional quality in crops can be enhanced either by adding new genes that supply the plants with more vitamins or minerals or by enhancing the expression of already present genes that are involved in nutrient biosynthesis (see Table 7). Transgenic techniques can be used to simultaneously incorporate genes that increase the concentration of micronutrients, their bioavailability and inhibit antinutritional factors (ANFs) in crops that restrict the utilization of nutrients (117). Transgenic approach presents a rational solution to improve the concentration and bioavailability of micronutrients (106, 118) especially when there is a limited genetic base present in different plant varieties (119, 120).
Table 7. Genes involved in micronutrient enrichment.
Scientists have used biotechnology to develop crops that are high in beta-carotene, a precursor of Vitamin A, iron and zinc which are essential for human health but often lacking in the diet of people in developing countries. One of the examples is the development of vitamin A-rich rice called “golden rice,” which could help to address vitamin A deficiency in developing countries. Additionally, biotechnology can be used to improve the quality of food by increasing its shelf life, enhancing its flavor, reducing its allergenicity and producing food ingredients with health benefits like functional proteins, fibers and lipids. These ingredients can be used to improve the nutritional value of food products, making them more healthful and beneficial for consumers. This can help to make food more accessible and affordable for consumers, particularly in areas where food is scarce or expensive. It is a promising approach to improve the nutritional value of crops, but it is also a controversial issue and further research is needed to fully understand its potential impacts and risks.
Challenges
There are several challenges that need to be overcome in order to effectively implement biofortification programs:
Limited availability of biofortified varieties: Many biofortified crops are still in the development or testing phase and may not yet be widely available for cultivation.
Limited awareness and understanding of biofortification: Many people may not be aware of the benefits of biofortified crops or may have misconceptions about their safety or nutritional value.
Limited distribution and access: Even if biofortified crops are available, they may not reach the people who need them most, due to factors such as inadequate infrastructure, lack of storage facilities, or high costs.
Political and regulatory challenges: The development and distribution of biofortified crops can be hindered by political and regulatory barriers, such as concerns about intellectual property rights, biosafety and trade issues. The development and commercialization of genetically modified (GM) crops, which are a potential tool for biofortification, can be subject to complex and often controversial regulations.
Agricultural constraints: Biofortified crops may not always perform as well as non-biofortified varieties under certain growing conditions, such as drought or pests.
Limited adoption: Even if biofortified crops are available, farmers may not choose to grow them if they are not familiar with the benefits or if they are not convinced that the crops will be more profitable.
Consumer acceptance: Biofortified crops may be perceived as being different or inferior to non-biofortified varieties, which could affect consumer acceptance.
Funding: Biofortification programs require ongoing funding in order to support research, development, and implementation efforts.
Coordination: Biofortification programs often involve multiple stakeholders, including governments, NGOs, farmers, and the private sector. Ensuring effective coordination among these stakeholders can be challenging.
Future prospects
The discipline of biofortification has a number of intriguing research areas that hold great potential for the future. It is becoming an increasingly important area of study as the global population continues to hike and the demand for nutrient-rich food is growing. Scientists are working on developing new varieties of crops that are high in essential vitamins and minerals, such as iron, zinc and vitamin A. As research in this field continues to advance, it is likely that we will see an increasing number of nutrient-rich crop varieties that can help to address global malnutrition and improve public health. Improved plant uptake and absorption of crucial nutrients is the subject of another field of biofortification research. This includes the use of fertilizers and other agricultural practices that can increase the availability of nutrients in the soil and enhance the plants’ ability to absorb them.
Overall, the future prospects for biofortification are very promising. Some potential benefits of biofortification include:
Expanding the range of biofortified crops: Currently, the main focus of biofortification has been on staple crops such as rice, wheat and maize, but there is potential to biofortify other crops as well, such as fruits, vegetables and legumes.
Improving the efficiency of biofortification: Scientists are working on ways to increase the nutrient content of crops using fewer resources, in order to make biofortification more cost-effective and sustainable.
Improving the distribution and access to biofortified crops: This may involve developing new storage and transport technologies, as well as working with governments and other organizations to create supportive policies and infrastructure.
Promoting the awareness and understanding of biofortification: This could involve educating the public about the benefits of biofortified crops and addressing any concerns or misconceptions about their safety or nutritional value.
Reducing malnutrition and improving public health: Biofortification can increase the nutrient value of locally-grown crops, which can help to address deficiencies in essential vitamins and minerals and improve the nutritional status of populations that rely on these crops as a major source of energy and nutrients and contribute to food security by increasing the availability of nutritious foods.
Supporting sustainable development: Biofortification can be implemented at a relatively low cost and can be integrated into existing farming practices, making it a sustainable and scalable solution for improving nutrition.
Improving gender equity: Women and children are often the most vulnerable to malnutrition, and biofortification can help to reduce gender disparities in access to nutritious foods.
Conclusion
Biofortification heralds a transformative paradigm in a battle against malnutrition and hidden hunger, which is often not visible to the naked eye, as people may appear well-nourished but still be deficient in essential vitamins and minerals. In some cases, biofortified crops may also have higher yields, which can help to improve food security and increase income for farmers. It can be a cost-effective and sustainable way to improve nutrition, as it relies on using existing agricultural infrastructure and practices. It can help to address dietary deficiencies and improve nutrition in low-income populations, which may not have the same access to nutrient-rich foods as those in higher-income groups. The integration of multi-nutrient biofortification and cutting-edge nano-technology marks a groundbreaking leap.
However, there are several challenges that need to be overcome in order to effectively implement biofortification programs, including limited availability of biofortified varieties, high costs of production, limited awareness and understanding, limited distribution and access, and political and regulatory barriers. Biofortified food crops have the potential to significantly improve the lives and health of millions of underprivileged people in India with careful planning, execution, and implementation while requiring a low investment in research.
Author contributions
First draft designed by Avnee, reviewed by SS, DC and reviewed and revised by PJ and RR. All authors contributed to the article and approved the submitted version.
Acknowledgments
Authors are thankful to PANF, CAAST, NAHEP-ICAR & World Bank funded project for providing technical and financial support in publishing the article.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher’s note
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References
1. Sheoran, S, Kumar, S, Ramtekey, V, Kar, P, Meena, RS, and Jangir, CK. Current status and potential of biofortification to enhance crop nutritional quality: an overview. Sustainability. (2022) 14:3301. doi: 10.3390/su14063301
2. Yadava, DV, Choudhary, PR, Hossain, F, Kumar, D, and Mohpatra, T. Biofortified varieties: Sustainable way to alleviate malnutrition. 3rd ed. New Delhi: Indian Council of Agricultural Research (2020).
3. Gomathi, M, Vethamoni, PI, and Gopinath, P. Biofortification in vegetable crops – a review. Chem Sci Rev Lett. (2017) 6:1227–37.
4. Bouis, HE, Hotz, C, McClafferty, B, Meenakshi, JB, and Pfeiffer, WH. Biofortification: a new tool to reduce micronutrient malnutrition. Food Nutr Bull. (2011) 32:S31–40. doi: 10.1177/15648265110321S105
5. Straeten, VD, Bhullar, D, De Steur, NK, et al. Multiplying the efficiency and impact of biofortification through metabolic engineering. Nat Commun. (2020) 11:5203. doi: 10.1038/s41467-020-19020-4
6. Ismail, AM, Heuer, S, Thomson, MJ, and Wissuwa, M. Genetic and genomic approaches to develop rice germplasm for problem soils. Plant Soil. (2007) 65:547–16. doi: 10.1007/s11103-007-9215-2
7. Bhardwaj, AK, Chejara, S, Malik, K, Kumar, R, Kumar, A, and Yadav, RK. Agronomic biofortification of food crops: an emerging opportunity for global food and nutritional security. Front Plant Sci. (2022) 13:1055278. doi: 10.3389/fpls.2022.1055278
8. Chandra, M, Kadam, P, Shaikh, C, and Geethanjali, D. Role of Nano-particles in agronomic biofortification In: Sustainable agriculture and food security. Chapter 5 Deepika Book Agency. (2023). 89–4.
9. Pasricha, SR, Drakesmith, H, Black, J, Hipgrave, D, and Biggs, BA. Control of iron deficiency anemia in low- and middle-income countries. Blood. (2013) 121:2607–17. doi: 10.1182/blood-2012-09-453522
10. NIH (National Institute of Health) Iron-fact sheet for health professionals. Available at: https://ods.od.nih.gov/factsheets/Iron-HealthProfessional/ (2022).
11. Wei, Y, Shohag, MJ, Yang, X, and Yibin, Z. Effects of foliar iron application on iron concentration in polished rice grain and its bioavailability. J Agric Food Chem. (2012) 60:11433–9. doi: 10.1021/jf3036462
12. Singh, P, Dhaliwal, SS, and Sadana, US. Iron enrichment of paddy grains through ferti-fortification. J Res Punjab Agric Univ. (2013) 50:32–8.
13. Meena, BL, Rattan, RK, Datta, SP, and Meena, MC. Effect of iron application on iron nutrition of aerobic rice grown in different soils. J Envir Biol. (2016) 37:1377–83. doi: 10.22438/jeb/37/6/mrn-337
14. Ramzan, Y, Hafeez, MB, Khan, S, Nadeem, M, Batool, S, and Ahmad, J. Biofortification with zinc and iron improves the grain quality and yield of wheat crop. Int J Plant Product. (2020) 14:501–16. doi: 10.1007/s42106-020-00100-w
15. Hussain, A, Rizwan, M, Ali, S, Rehman, MZU, Qayyum, MF, Nawaz, R, et al. Combined use of different nanoparticles effectively decreased cadmium (cd) concentration in grains of wheat grown in a field contaminated with cd. Ecotoxicol Environ Saf. (2021) 215:112139. doi: 10.1016/j.ecoenv.2021.112139
16. Ali, B, Ali, A, Tahir, M, and Ali, S. Growth, seed yield and quality of mungbean as influenced by foliar application of iron sulfate. Pak J Life Soc Sci. (2014) 12:20–5.
17. Márquez-Quiroz, C, De-la-Cruz-Lázaro, E, Osorio-Osorio, R, and Sánchez-Chávez, E. Biofortification of cowpea beans with iron: Iron’s influence on mineral content and yield. J Soil Sci Plant Nutr. (2015) 15:839–47. doi: 10.4067/S0718-95162015005000058
18. Hidoto, L, Worku, W, Mohammed, H, and Taran, B. Effects of zinc application strategy on zinc content and productivity of chickpea grown under zinc deficient soils. J Soil Sci Plant Nutr. (2017) 17:112–6. doi: 10.4067/S0718-95162017005000009
19. Dhaliwal, SS, Sharma, V, Shukla, AK, Kaur, J, et al. Enrichment of zinc and iron micronutrients in lentil (Lens culinaris Medik.) through biofortification. Molecules. (2021) 26:7671. doi: 10.3390/molecules26247671
20. Kromann, P, Valverde, F, Alvarado, S, Vélez, R, Pisuña, J, et al. Can Andean potatoes be agronomically biofortified with iron and zinc fertilizers? Plant Soil. (2017) 411:121–8. doi: 10.1007/s11104-016-3065-0
21. Giordano, M, El-Nakhel, C, Pannico, A, Kyriacou, M, Stazi, SR, Pascale, SD, et al. Iron biofortification of red and green pigmented lettuce in closed soilless cultivation impacts crop performance and modulates mineral and bioactive composition. Agronomy. (2019) 9:290. doi: 10.3390/agronomy9060290
22. Gioia, FD, Petropoulos, SA, Hampton, MO, Morgan, K, and Rosskopf, EN. Zinc and iron agronomic biofortification of brassicaceae microgreens. Agronomy. (2019) 9:677–7. doi: 10.3390/agronomy9110677
23. Gibson, RS. Zinc deficiency and human health: etiology, health consequences, and future solutions. Plant Soil. (2012) 361:291–9. doi: 10.1007/s11104-012-1209-4
24. Cakmak, I, and Kutman, UB. Agronomic biofortification of cereals with zinc: a review. Euro J Soil Sci. (2018) 69:172–80. doi: 10.1111/ejss.12437
25. Shukla, A, and Behera, SK. Micronutrient research in India: retrospect and prospects. Preprints of seminar papers-2017 under AICRP on micronutrients (2018). doi: 10.13140/RG.2.2.20370.76489,
26. Wessells, KR, and Brown, KH. Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS One. (2012) 7:1–11. doi: 10.1371/journal.pone.0050568
27. Faujdar, RS, Sharma, M, Solanki, RL, and Dangi, RC. Effect of FYM, biofertilizers and zinc on yield and micronutrients uptake in maize. Asian J Soil Sci. (2014) 9:121–5.
28. Shivay, YS. Role of agronomic biofortification in alleviating malnutrition. Int J Econ Plants. (2015) 2:153–8.
29. Singh, A, and Shivay, YS. Effects of green manures and zinc fertilizer sources on DTPA-extractable zinc in soil and zinc content in basmati rice plants at different growth stages. Pedosphere. (2019) 29:504–5. doi: 10.1016/S1002-0160(17)60442-9
30. Ghasal, PC, Shivay, YS, Pooniya, V, Choudhary, M, and Verma, RK. Zinc partitioning in basmati rice varieties as influenced by Zn fertilization. Crop J. (2018) 6:136–7. doi: 10.1016/j.cj.2017.09.001
31. Prasad, R, and Shivay, YS. Relative grain zinc loading ability of cereals (rice, wheat, maize) and a grain legume (chickpea). Indian J Agric Sci. (2018) 88:307–3. doi: 10.56093/ijas.v88i2.79223
32. Ghasal, PC, Shivay, YS, Pooniya, V, Choudhary, M, and Verma, RK. Response of wheat genotypes to zinc fertilization for improving productivity and quality. Arch Agron Soil Sci. (2017) 63:1597–12. doi: 10.1080/03650340.2017.1289515
33. Firdous, S, Agarwal, BK, and Chhabra, V. Zinc-fertilization effects on wheat yield and yield components. J Pharmacog Phytochem. (2018) 7:3497–9.
34. Elhaj, BZ, and Unrine, JM. Functionalized-ZnO-nanoparticle seed treatments to enhance growth and Zn content of wheat (Triticum aestivum) seedlings. J Agric Food Chem. (2018) 66:12166–78. doi: 10.1021/acs.jafc.8b03277
35. Dhaliwal, SS, Ram, H, Shukla, AK, and Mavi, GS. Zinc biofortification of bread wheat, triticale, and durum wheat cultivars1by foliar zinc fertilization. J Plant Nutr. (2019) 42:813–22. doi: 10.1080/01904167.2019.1584218
36. Tabassum, S, Jeet, S, Kumar, R, Dev, CM, et al. Effect of organic manure and zinc fertilization on zinc transformation and biofortification of crops in Vertisols of Central India. J Agric Sci. (2014) 6:221–1. doi: 10.5539/jas.v6n8p221
37. Behera, SK, Shukla, AK, Tiwari, PK, Tripathi, A, et al. Classification of pigeonpea [Cajanus cajan (L.) Millsp.] genotypes for zinc efficiency. Plan Theory. (2020) 9:952. doi: 10.3390/plants9080952
38. Roy, N, and Ghosh, K. Enhancing nutrient availability, yield and quality of safflower (Carthamus tinctorius L.) through zinc and Sulphur in Alfisol. J Pharmacog Phytochem. (2020) 9:693–7.
39. Dhaliwal, SS, Sharma, V, Verma, V, Singh, H, Singh, P, and Kaur, K. Biofortification of linseed (Linum usitatissimum L.) through mineral and chelated forms of Zn on yield, Zn accumulation, quality parameters, efficiency indices and economic under low Zn soils of North-Western India. J Plant Nutr. (2023) 46:356–9. doi: 10.1080/01904167.2022.2068435
40. Rugeles-Reyes, SM, AB, C, Lopez Aguilar, MA, and Silva, PH. Foliar application of zinc in the agronomic biofortification of arugula. Food Sci Technol. (2019) 39:1011–7. doi: 10.1590/fst.12318
41. Almeida, HJ, Vergara Carmona, VM, Ferreira, IM, Furtini, AE, Cecílio, AB, and Mauad, M. Soil type and zinc doses in agronomic biofortification of lettuce genotypes. Agronomy. (2020) 10:124. doi: 10.3390/agronomy10010124
42. Rivera-Martin, A, Broadley, MR, and Poblaciones, MJ. Soil and foliar zinc application to biofortify broccoli (Brassica oleracea var. italica L.): effects on the zinc concentration and bioavailability. Plant Soil Environ. (2020) 66:113–8. doi: 10.17221/14/2020-PSE
43. Liu, M, Xu, M, Yu, H, Fu, H, Tang, S, Ma, Q, et al. Spraying ZnEDTA at high concentrations: an ignored potential for producing zinc-fortified pear (Pyrus spp.) fruits without causing leaf and fruitlet burns. Sci Hortic. (2023) 322:112380. doi: 10.1016/j.scienta.2023.112380
44. Guevara, JEM, Sanches, AG, Pedrosa, VMD, Cruz, MCP, Silva, JA, and Teixeira, GH. The injection of zinc sulfate into banana tree pseudostem can triple the zinc content and it is an effective method for fruit biofortification. J Food Compos Anal. (2021) 102:104020. doi: 10.1016/j.jfca.2021.104020
45. Smoleń, S, Wierzbińska, J, Sady, W, Kołton, A, Wiszniewska, A, and Liszka-Skoczylas, M. Iodine biofortification with additional application of salicylic acid affects yield and selected parameters of chemical composition of tomato fruits (Solanum lycopersicum L.). Sci Hortic. (2015) 188:89–96. doi: 10.1016/j.scienta.2015.03.023
46. Li, R, Li, DW, Liu, HP, Hong, CL, Song, MY, Dai, ZX, et al. Enhancing iodine content and fruit quality of pepper (Capsicum annuum L.) through biofortification. Sci Hortic. (2017) 214:165–3. doi: 10.1016/j.scienta.2016.11.030
47. Ojok, J, Omara, P, Opolot, E, Odongo, W, Olum, S, Gijs, DL, et al. Iodine agronomic biofortification of cabbage (Brassica oleracea var. capitata) and cowpea (Vigna unguiculata L.) is effective under farmer field conditions. Agronomy. (2019) 9:797. doi: 10.3390/agronomy9120797
48. Dobosy, P, Endrédi, A, Sandil, S, Vetési, V, Rékási, M, Takács, T, et al. Biofortification of potato and carrot with iodine by applying different soils and irrigation with iodine-containing water. Front Plant Sci. (2020) 11:1716. doi: 10.3389/fpls.2020.593047
49. Smoleń, LI, Smoleń, S, Rożek, S, Sady, W, and Strzetelski, P. Iodine biofortification of potato (Solanum tuberosum L.) grown in field. Agronomy. (2020) 10:1916. doi: 10.3390/agronomy10121916
50. Budke, C, Dierend, W, Schön, HG, Hora, K, Hermann, MK, and Diemo, D. Iodine biofortification of apples and pears in an orchard using foliar sprays of different composition. Front Plant Sci. (2021) 12:638671. doi: 10.3389/fpls.2021.638671
51. Ligowe, IS, Bailey, EH, Young, SD, Ander, EL, Kabambe, V, Chilimba, AD, et al. Agronomic iodine biofortification of leafy vegetables grown in Vertisols, Oxisols and Alfisols. Environ Geochem Health. (2021) 43:361–4. doi: 10.1007/s10653-020-00714-z
52. Puccinelli, M, Landi, M, Maggini, R, Pardossi, A, and Incrocci, L. Iodine biofortification of sweet basil and lettuce grown in two hydroponic systems. Sci Hortic. (2021) 276:109783. doi: 10.1016/j.scienta.2020.109783
54. WHO (2007) Iodine deficiency in Europe: a continuing public health problem. Available at: https://www.who.int/publications/i/item/9789241593960
55. Rayman, MP. Selenium and human health. Lancet. (2012) 379:1256–68. doi: 10.1016/S0140-6736(11)61452-9
56. White, PJ, and Brown, PH. Plant nutrition for sustainable development and global health. Ann Bot Lond. (2010) 105:1073–80. doi: 10.1093/aob/mcq085
57. Boldrin, PF, Faquin, V, Ramos, SJ, Guilherme, LRG, Bastos, CEA, Carvalho, GS, et al. Selenato e selenito na produção e biofortificação agronômica com selênio em arroz. Pesqui Agropecu Bras. (2012) 47:831–7. doi: 10.1590/S0100-204X2012000600014
58. Ramos, S, Faquin, V, Guilherme, L, Castro, EM, Ávila, F, and Carvalho, G. Selenium biofortification and antioxidante activity in lettuce plants feed with selenate and selenite. Plant Soil Environ. (2011) 56:583–7.
59. Poblaciones, MJ, Rodrigo, S, Santamaria, O, Chen, Y, and McGrath, SP. Selenium accumulation and speciation in biofortified chickpea (Cicer arietinum L.) under Mediterranean conditions. J Sci Food Agric. (2014) 94:1101–6. doi: 10.1002/jsfa.6372
60. Yang, F, Chen, L, Hu, Q, and Pan, G. Effect of the application of selenium on selenium content of soybean and its products. Biol Trace Elem Res. (2003) 93:249–6. doi: 10.1385/BTER:93:1-3:249
61. Rahman, MM, Erskine, W, Materne, MA, McMurray, LM, Thavarajah, P, Thavarajah, D, et al. Enhancing selenium concentration in lentil (Lens culinaris subsp. culinaris) through foliar application. J Agric Sci. (2015) 153:656–5. doi: 10.1017/S0021859614000495
62. Yasin, M, El Mehdawi, AF, Jahn, CE, Anwar, A, Turner, MF, Faisal, M, et al. Seleniferous soils as a source for production of selenium-enriched foods and potential of bacteria to enhance plant selenium uptake. Plant Soil. (2015) 386:385–4. doi: 10.1007/s11104-014-2270-y
63. Bañuelos, GS, Arroyo, IS, Dangi, SR, and Zambrano, MC. Continued selenium biofortification of carrots and broccoli grown in soils once amended with se-enriched S. pinnata. Front Plant Sci. (2016) 7:1251. doi: 10.3389/fpls.2016.01251
64. Smoleń, S, Skoczylas, Ł, Ledwożyw-Smoleń, I, Rakoczy, R, Kopeć, A, Piątkowska, E, et al. Biofortification of carrot (Daucus carota L.) with iodine and selenium in a field experiment. Front Plant Sci. (2016) 7:730. doi: 10.3389/fpls.2016.00730
65. Li, X, Wu, Y, Li, B, Yang, Y, and Yang, Y. Selenium accumulation characteristics and biofortification potentiality in turnip (Brassica rapa var. rapa) supplied with selenite or selenate. Front Plant Sci. (2018) 8:2207. doi: 10.3389/fpls.2017.02207
66. Woch, W, and Hawrylak-Nowak, B. Selected antioxidant properties of alfalfa, radish, and white mustard sprouts biofortified with selenium. Acta Agrobot. (2019) 72:1768. doi: 10.5586/aa.1768
67. Smoleń, S, Baranski, R, Ledwożyw-Smoleń, I, Skoczylas, L, and Sady, W. Combined biofortification of carrot with iodine and selenium. Food Chem. (2019) 300:125202. doi: 10.1016/j.foodchem.2019.125202
68. Skoczylas, Ł, Tabaszewska, M, Smoleń, S, Słupski, J, Liszka-Skoczylas, M, and Barański, R. Carrots (Daucus carota L.) biofortified with iodine and selenium as a raw material for the production of juice with additional nutritional functions. Agronomy. (2020) 10:1360. doi: 10.3390/agronomy10091360
69. Ávila, FW, Faquin, V, Yang, Y, Ramos, SJ, Guilherme, LR, Thannhauser, TW, et al. Assessment of the anticancer compounds se-methylselenocysteine and glucosinolates in se-biofortified broccoli (Brassica oleracea L. var. italica) sprouts and florets. J Agric Food Chem. (2013) 61:6216–23. doi: 10.1021/jf4016834
70. Oancea, A, Gaspar, A, Seciu, AM, Stefan, LM, Craciunescu, O, Georgescu, F, et al. Development of a new technology for protective biofortification with selenium of Brassica crops. AgroLife Sci J. (2015) 4:80–5.
71. Bañuelos, GS, Arroyo, IS, Pickering, IJ, Yang, SI, and Freeman, JL. Selenium biofortification of broccoli and carrots grown in soil amended with se-enriched hyperaccumulator Stanleya pinnata. Food Chem. (2015) 166:603–8. doi: 10.1016/j.foodchem.2014.06.071
72. Bachiega, P, Salgado, JM, de Carvalho, JE, Lúcia, A, Ruiz, TG, Schwarz, K, et al. Antioxidant and antiproliferative activities in different maturation stages of broccoli (Brassica oleracea Italica) biofortified with selenium. Food Chem. (2016) 190:771–6. doi: 10.1016/j.foodchem.2015.06.024
73. Liaoa, X, Raoa, S, Yub, T, Zhub, Z, Yanga, X, Xued, H, et al. Selenium yeast promoted the se accumulation, nutrient quality and antioxidant system of cabbage (Brassica oleracea var. capitata L.). Plant Signal Behav. (2021) 6:1907042–50. doi: 10.1080/15592324.2021.1907042
74. Golob, A, Kroflič, A, Jerše, A, Kacjan Maršić, N, Šircelj, H, Stibilj, V, et al. Response of pumpkin to different concentrations and forms of selenium and iodine, and their combinations. Plan Theory. (2020) 9:899. doi: 10.3390/plants9070899
75. Ríos, JJ, Rosales, MA, Blasco, B, Cervilla, LM, Romero, L, and Ruiz, JM. Biofortification of se and induction of the antioxidant capacity in lettuce plants. Sci Hortic. (2008) 116:248–5. doi: 10.1016/j.scienta.2008.01.008
76. Smoleń, S, Kowalska, I, and Sady, W. Assessment of biofortification with iodine and selenium of lettuce cultivated in the NFT hydroponic system. Sci Hortic. (2014) 166:9–16. doi: 10.1016/j.scienta.2013.11.011
77. Narvaez-Ortiz, W, Becvort-Azcurra, A, Fuentes-Lara, L, Benavides-Mendoza, A, Valenzuela-García, J, and Gonzalez, FJ. Mineral composition and antioxidant status of tomato with application of selenium. Agronomy. (2018) 8:185. doi: 10.3390/agronomy8090185
78. Rahim, FP, Rocio, CG, Adalberto, BM, Lidia Rosaura, SC, and Maginot, NH. Agronomic biofortification with selenium in tomato crops (Solanum lycopersicon L. mill). Agriculture. (2020) 10:486. doi: 10.3390/agriculture10100486
79. Sabatino, L, La Bella, S, Georgia, N, Giovanni, I, Fabio, D, Claudio, P, et al. Selenium biofortification and grafting modulate plant performance and functional features of cherry tomato grown in a soilless system. Sci Hortic. (2021) 285:110095. doi: 10.1016/j.scienta.2021.110095
80. Schiavon, M, Lima, LW, Jiang, Y, and Hawkesford, MJ. (2017). Effects of selenium on plant metabolism and implications for crops and consumers. In: Selenium in plants Molecular, Physiological, Ecological and Evolutionary Aspects Edition: 1 Chapter: eds. EAH Pilon-Smits, LHE Winkel, and ZQ Lin. 15 Springer International Publisher.
81. Abdoli, M. (2020) Effects of micronutrient fertilization on the overall quality of crops. In: Plant Micronutrients, Deficiency and Toxicity Management Edition: Chapter: 2 eds. T Aftab and KR Hakeem. Springer, Cham.
82. Piekarska, AD, Kołodziejski, T, Pilipczuk, M, Bodnar, P, Konieczka, B, Kusznierewicz, FS, et al. The influence of selenium addition during germination of Brassica seeds on health-promoting potential of sprouts. Int J Food Sci Nutr. (2014) 65:692–2. doi: 10.3109/09637486.2014.917148
83. Revelou, PK, Xagoraris, M, Kokotou, MG, and Constantinou-Kokotou, V. Cruciferous vegetables as functional foods: effects of selenium biofortification. Int J Veg Sci. (2022) 28:191–16. doi: 10.1080/19315260.2021.1957052
84. Gui, JY, Rao, S, Huang, X, Liu, X, Cheng, S, and Xu, F. Interaction between selenium and essential micronutrient elements in plants: a systematic review. Sci Total Environ. (2022) 853:158673. doi: 10.1016/j.scitotenv.2022.158673
85. Szerement, J, Szatanik-Kloc, A, Mokrzycki, J, et al. Agronomic biofortification with se, Zn, and Fe: an effective strategy to enhance crop nutritional quality and stress defense—a review. J Soil Sci Plant Nutr. (2022) 22:1129–59. doi: 10.1007/s42729-021-00719-2
86. Aziz, AM, Shehab, DA, and Abdulrazak, MA. Antioxidant categories and mode of action. Antioxidants. London: IntechOpen (2019).
87. Valença, AW, Bake, A, Brouwer, ID, and Giller, KE. Agronomic biofortification of crops to fight hidden hunger in sub-Saharan Africa. Glob Food Sec. (2017) 12:8–14. doi: 10.1016/j.gfs.2016.12.001
88. Amira, SS, AEl-Feky, S, and Essam, D. Alleviation of salt stress on Moringa peregrina using foliar application of nanofertilizers. J Hortic For. (2015) 7:36–47. doi: 10.5897/JHF2014.0379
89. Noreen, S, Sultan, M, Akhter, MS, Shah, KH, Ummara, U, Manzoor, H, et al. Foliar fertigation of ascorbic acid and zinc improves growth, antioxidant enzyme activity and harvest index in barley (Hordeum vulgare L.) grown under salt stress. Plant Physiol Biochem. (2020) 158:244–4. doi: 10.1016/j.plaphy.2020.11.007
90. Sida-Arreola, JP, Sánchez, E, Preciado-Rangel, P, and Márquez-Quiroz, C. Does zinc biofortification affects the antioxidant activity in common bean? Cogent Food Agric. (2017) 3:1283725. doi: 10.1080/23311932.2017.1283725
91. Dhaliwal, SS, Sharma, V, Shukla, AK, Kaur, M, Verma, V, Singh, SP, et al. Biofortification of oil quality, yield, and nutrient uptake in Indian mustard (Brassica juncea L.) by foliar application of boron and nitrogen. Front Plant Sci. (2022) 13:976391. doi: 10.3389/fpls.2022.976391
92. Rivera-Martin, A, Reynolds-Marzal, D, Martin, A, Velazquez, R, and Poblaciones, MJ. Combined foliar zinc and nitrogen application in broccoli (Brassica oleracea var. italica L.): effects on growth, nutrient bioaccumulation, and bioactive compounds. Agronomy. (2021) 11:548. doi: 10.3390/agronomy11030548
93. Montoya, S, Ortega, E, Navarro, E, and Lorenzo, ML. CUCUMBER BIOFORTIFICATION WITH POTASSIUM. Eur. Sci. J. (2013) 9:101–108.
94. Shankar, KS, SumaK, CKB, Kumar, AP, Grover, M, Mekala, S, Sankar, M, et al. Improving phytochemical and nutritional quality of spinach (Spinacia oleracea) through phosphate solubilizing Bacteria. Indian J Dryland Agric Res Dev. (2014) 29:104–7. doi: 10.5958/2231-6701.2014.01224.X
95. Hawrylak-Nowak, B, Dresler, S, Rubinowska, K, Matraszek-Gawron, R, Woch, W, and Hasanuzzaman, M. Selenium biofortification enhances the growth and alters the physiological response of lamb's lettuce grown under high-temperature stress. Plant Physiol Biochem. (2018) 127:446–6. doi: 10.1016/j.plaphy.2018.04.018
96. Gaucin-Delgado, J, Hernandez-Montiel, GL, Sánchez-Chávez, E, Ortiz, H, Fortis-Hernández, M, Reyes-Pérez, J, et al. Agronomic biofortification with selenium improves the yield and nutraceutical quality in tomato under soilless conditions. Notulae Botanicae Horti Agrobotanici Cluj-Napoca. (2020) 48:1221–32. doi: 10.15835/nbha48312000
97. Kaur, K, Sohu, VS, Sharma, A, Srivastava, P, Mavi, GS, Kaur, H, et al. Biofortification strategies to increase wheat nutrition and sustaining yield simultaneously. Ind J Genet Plant Breed. (2019) 79:15–24. doi: 10.31742/IJGPB.79.1.3
98. Rao, S, Neeraja, CN, Madhu Babu, P, Nirmala, B, Suman, K, Rao, LVS, et al. Zinc biofortified Rice varieties: challenges, possibilities, and Progress in India. Front Nutr. (2020) 7:26. doi: 10.3389/fnut.2020.00026
99. Harvest plus. Biofortified crops released. (2022). Available at: https://bcr.harvestplus.org/varieties_released_list?crop
100. Mandal, NP, Dipankar, M, Somnath, R, Banerjee, A, Singh, C, and Variar, M. Rainfed upland rice: activities, achievements and aspirations. Cuttack: ICAR-National Rice Research Institute (2019).
101. Korram, G, Samadhiya, VK, Bhagat, AS, and Pradhan, AK. Assessment on quality parameters (protein, carbohydrate, hulling, milling and HRR) of traditional short grain aromatic rice, high yielding scented rice and fortified rice under organic farming. Pharma Innov J. (2022) 11:1792–4.
102. Yadava, DK, Hossain, F, and Mohapatra, T. Nutritional security through crop biofortification in India: status & future prospects. Indian J Med Res. 148:621–1. doi: 10.4103/ijmr.IJMR_1893_18
103. Yadava, DK, Choudhury, PR, Hossain, F, Kumar, D, and Mohapatra, T. Biofortified varieties: sustainable way to alleviate malnutrition (second edition). New Delhi: Indian Council of Agricultural Research (2019). 44 p.
104. ICRISAT India gets its first biofortified sorghum – ICRISAT. Available at: https://www.icrisat.org/india-gets-its-first-biofortified-sorghum/ (2018).
105. Nestel, P, Bouis, HE, Meenakshi, JV, and Pfeiffer, W. Biofortification of staple food crops. J Nutr. (2006) 136:1064–7. doi: 10.1093/jn/136.4.1064
106. Prasad, BVG, Mohanta, S, Rahaman, S, and Bareily, P. Bio-fortification in horticultural crops. J Agric Eng Food Technol. (2015) 2:95–9.
107. Pezeshki, A, Zapata, RC, Singh, A, Yee, NJ, and Chelikani, PK. Low protein diets produce divergent effects on energy balance. Sci Rep. (2016) 28:25145. doi: 10.1038/srep25145
108. Hodge, C, and Taylor, C. Vitamin a deficiency in: StatPearls [internet]. Treasure Island (FL): StatPearls Publishing (2023).
109. Hansen, TH, Lombi, E, Fitzgerald, M, and Laursen, HK. Losses of essential mineral nutrients by polishing of rice differ among genotypes due to contrasting grain hardness and mineral distribution. J Cereal Sci. (2012) 56:307–5. doi: 10.1016/j.jcs.2012.07.002
110. Kamble, U, Mishra, CN, Govindan, V, Sharma, AK, Pawar, S, Kumar, S, et al. Ensuring nutritional security in India through wheat biofortification: a review. Genes. (2022) 13:2298. doi: 10.3390/genes13122298
111. Phougat, D, and Sethi, SK. Wheat biofortification: agricultural investment to refrain malnutrition especially in developing world. J Entomol Zool Stud. (2016) 7:506–1.
112. Wani, SH, Gaikwad, K, Razzaq, A, Samantara, K, Kumar, M, and Govindan, V. Improving zinc and iron biofortification in wheat through genomics approaches. Mol Biol Rep. (2022) 49:8007–23. doi: 10.1007/s11033-022-07326-z
113. Msungu, SD, Mushongi, AA, Venkataramana, PB, and Mbega, ER. A review on the trends of maize biofortification in alleviating hidden hunger in sub-Sahara Africa. Sci Hortic. (2022) 299:111029. doi: 10.1016/j.scienta.2022.111029
114. Nkhata, SG, Chilungo, S, Memba, A, and Mponela, P. Biofortification of maize and sweet potatoes with provitamin a carotenoids and implication on eradicating vitamin a deficiency in developing countries. J Agric Food Res. (2020) 2:100068. doi: 10.1016/j.jafr.2020.100068
115. Matongera, GN, Thokozile, N, Cosmos, M, Casper, K, Angeline, B, and Maryke, L. Multinutrient biofortification of maize (Zea mays L) in Africa: current status, opportunities and limitations. Nutrients. (2021) 13:1039. doi: 10.3390/nu13031039
116. Nuss, ET, and Tanumihardjo, SA. Quality protein maize for Africa: closing the protein inadequacy gap in vulnerable populations. Adv Nutr. (2011) 2:217–4. doi: 10.3945/an.110.000182
117. Garg, M, Sharma, N, Sharma, S, Kapoor, P, Kumar, A, Chunduri, V, et al. Biofortified crops generated by breeding, agronomy, and transgenic approaches are improving lives of millions of people around the world. Front Nutr. (2018) 5:12. doi: 10.3389/fnut.2018.00012
118. Rehan, SA, and Singh, P. Biofortification: enriching vegetable crops with nutrients to reduce global hunger. Int J Curr Microbiol App Sci. (2020) 11:2499–11.
119. Brinch-Pedersen, H, Borg, S, Tauris, B, and Holm, PB. Molecular genetic approaches to increasing mineral availability and vitamin content of cereals. J Cereal Sci. (2007) 46:308–6. doi: 10.1016/j.jcs.2007.02.004
120. Zhu, C, Naqvi, S, Gomez-Galera, S, Pelacho, AM, Capell, T, and Christou, P. Transgenic strategies for the nutritional enhancement of plants. Trends Plant Sci. (2007) 12:548–5. doi: 10.1016/j.tplants.2007.09.007
121. Connorton, JM, Jones, ER, Rodríguez-Ramiro, I, Fairweather-Tait, S, Uauy, C, and Balk, J. Wheat vacuolar Iron transporter TaVIT2 transports Fe and Mn and is effective for biofortification. Plant Physiol. (2017) 174:2434–44. doi: 10.1104/pp.17.00672
122. Malik, M, Pandey, S, Tripati, K, Yaqoob, U, and Kaul, T. Biofortification strategies for enhancing grain zinc and iron levels in wheat. Int J Microbiol Biochem Mol Biol. (2016) 2:07–10.
123. Tamás, C, Kisgyörgy, BN, Rakszegi, M, Wilkinson, MD, Yang, M-S, and Láng, L. Transgenic approach to improve wheat (Triticum aestivum L.) nutritional quality. Plant Cell Rep. (2009) 28:1085–94. doi: 10.1007/s00299-009-0716-0
124. Wang, C, Zeng, J, Li, Y, Hu, W, Chen, L, and Miao, Y. Enrichment of provitamin a content in wheat (Triticum aestivum L.) by introduction of the bacterial carotenoid biosynthetic genes CrtB and CrtI. J Exp Bot. (2014) 65:2545–56. doi: 10.1093/jxb/eru138
125. Borg, S, Brinch-Pedersen, H, Tauris, B, Madsen, LH, Darbani, B, Noeparvar, S, et al. Wheat ferritins: improving the iron content of the wheat grain. J Cereal Sci. (2012) 56:204–3. doi: 10.1016/j.jcs.2012.03.005
126. Mir, Z, Yadav, P, Ali, S, and Sharma, S. Transgenic biofortified crops: applicability and challenges In: TR Sharma, R Deshmukh, and H Sonah, editors. Advances in Agri-food biotechnology. Singapore: Springer Verlag (2020)
127. Inoue, H, Kyoko, H, Michiko, T, Hiromi, N, Satoshi, M, and Naoko, N. Three rice nicotianamine synthase genes, OsNAS1, OsNAS2, and OsNAS3 are expressed in cells involved in long-distance transport of iron and differentially regulated by iron. Plant J. (2003) 36:366–1. doi: 10.1046/j.1365-313X.2003.01878.x
128. Kawakami, Y, and Bhullar, NK. Molecular processes in iron and zinc homeostasis and their modulation for biofortification in rice. J Integr Plant Biol. (2018) 60:1181–98. doi: 10.1111/jipb.12751
129. Zhang, Y, Xu, YH, Yi, HY, and Gong, JM. Vacuolar membrane transporters OsVIT1 and OsVIT2 modulate iron translocation between flag leaves and seeds in rice. Plant J. (2012) 72:400–16. doi: 10.1111/j.1365-313X.2012.05088.x
130. Sundararajan, S, Rajendran, V, Sivakumar, HP, Nayeem, S, Chandra, HM, Sharma, A, et al. Enhanced vitamin E content in an Indica rice cultivar harbouring two transgenes from Arabidopsis thaliana involved in tocopherol biosynthesis pathway. Plant Biotechnol J. (2021) 19:1083–5. doi: 10.1111/pbi.13578
131. Strobbe, S, Verstraete, J, Stove, C, and Van Der Straeten, D. Metabolic engineering of rice endosperm towards higher vitamin B1 accumulation. Plant Biotechnol J. (2021) 19:1253–67. doi: 10.1111/pbi.13545
132. Mangel, N, Fudge, JB, Li, KT, Wu, TY, Tohge, T, Fernie, AR, et al. Enhancement of vitamin B6 levels in rice expressing Arabidopsis vitamin B6 biosynthesis de novo genes. Palestine-lsrael J. (2019) 99:1047–65.
133. Blancquaert, D, Van Daele, J, Strobbe, S, Kiekens, F, Storozhenko, S, De Steur, H, et al. Improving folate (vitamin B 9) stability in biofortified rice through metabolic engineering. Nat Biotechnol. (2015) 33:1076–8. doi: 10.1038/nbt.3358
134. Trijatmiko, KR, Dueñas, C, Tsakirpaloglou, N, Torrizo, L, Arines, FM, Adeva, C, et al. Biofortified indica rice attains iron and zinc nutrition dietary targets in the field. Sci Rep. (2016) 6:19792. doi: 10.1038/srep19792
135. Ogo, Y, Ozawa, K, Ishimaru, T, Murayama, T, and Takaiwa, F. Transgenic rice seed synthesizing diverse flavonoids at high levels: a new platform for flavonoid production with associated health benefits. Plant Biotechnol J. (2013) 11:734–6. doi: 10.1111/pbi.12064
136. Decourcelle, M, Perez-Fons, L, Baulande, S, Steiger, S, Couvelard, L, Hem, S, et al. Combined transcript, proteome, and metabolite analysis of transgenic maize seeds engineered for enhanced carotenoid synthesis reveals pleotropic effects in core metabolism. J Exp Bot. (2015) 66:3141–50. doi: 10.1093/jxb/erv120
137. Kumar, K, Gambhir, G, Dass, A, Tripathi, AK, Singh, A, Jha, AK, et al. Genetically modified crops: current status and future prospects. Planta. (2020) 251:91. doi: 10.1007/s00425-020-03372-8
138. Lipkie, TE, De Moura, FF, Zhao, ZY, Albertsen, MC, Che, P, Glassman, K, et al. Bioaccessibility of carotenoids from transgenic provitamin a biofortified sorghum. J Agric Food Chem. (2013) 61:5764–71. doi: 10.1021/jf305361s
139. Holme, IB, Dionisio, G, Brinch-Pedersen, H, Wendt, T, Madsen, CK, Vincze, E, et al. Cisgenic barley with improved phytase activity. Plant Biotechnol J. (2012) 10:237–7. doi: 10.1111/j.1467-7652.2011.00660.x
140. Burton, RA, Collins, HM, Kibble, NA, Smith, JA, Shirley, NJ, Jobling, SA, et al. Over-expression of specific HvCslF cellulose synthase-like genes in transgenic barley increases the levels of cell wall (1, 3, 1, 4)-β-dglucans and alters their fine structure. Plant Biotechnol J. (2011) 9:117–5. doi: 10.1111/j.1467-7652.2010.00532.x
141. Newton, IS. Long-chain polyunsaturated fatty acids—the new frontier in nutrition. Lipid Technol. (1998) 10:77–81.
142. Fujisawa, M, Watanabe, M, Choi, SK, Teramoto, M, Ohyama, K, and Misawa, N. Enrichment of carotenoids in flaxseed (Linumu sitatissimum) by metabolic engineering with introduction of bacterial phytoene synthase gene crtB. J Biosci Bioeng. (2008) 105:636–1. doi: 10.1263/jbb.105.636
143. Newell-McGloughlin, M. Nutritionally improved agricultural crops. Plant Physiol. (2008) 147:939–3. doi: 10.1104/pp.108.121947
144. Falco, SC, Guida, T, Locke, M, Mauvais, J, Sanders, C, Ward, RT, et al. Transgenic canola and soybean seeds with increased lysine. Nat Biotechnol. (1995) 13:577–2. doi: 10.1038/nbt0695-577
145. Hong, H, Datla, N, Reed, DW, Covello, PS, MacKenzie, SL, and Qiu, X. High-level production of γ-linolenic acid in Brassica juncea using a Δ6 desaturase from pythium irregular. Plant Physiol. (2002) 129:354–2. doi: 10.1104/pp.001495
146. Pierce, EC, LaFayette, PR, Ortega, MA, Joyce, BL, Kopsell, DA, and Parrott, WA. Ketocarotenoid production in soybean seeds through metabolic engineering. PLoS One. (2015) 10:e0138196. doi: 10.1371/journal.pone.0138196
147. Sun, L, Yuan, B, Zhang, M, Wang, L, Cui, M, Wang, Q, et al. Fruit-specific RNAi-mediated suppression of SlNCED1 increases both lycopene and b-carotene contents in tomato fruit. J Exp Bot. (2012) 63:3097–08. doi: 10.1093/jxb/ers026
148. Thakur, V, Sharma, A, Sharma, P, Kumar, P, and Shilpa,. Biofortification of vegetable crops for vitamins, mineral and other quality traits. J Hortic Sci Biotechnol. (2022) 97:417–8. doi: 10.1080/14620316.2022.2036254
149. Cermak, T, Baltes, NJ, Cegan, R, Zhang, Y, and Voytas, DF. High-frequency, precise modification of the tomato genome. Genome Biol. (2015) 16:1–14. doi: 10.1186/s13059-015-0796-9
150. Maligeppagol, M, Chandra, GS, Navale, PM, and Kumar, NK. Anthocyanin enrichment of tomato (Solanum lycopersicum L.) fruit by metabolic engineering. Curr Sci. (2013) 105:72–80.
151. Halka, M, Smolen, S, Czernicka, M, Klimek-Chodacka, M, Pitala, J, and Tutaj, K. Iodine biofortification through expression of HMT, SAMT and S3H genes in Solanum lycopersicum L. Plant Physiol Biochem. (2019) 144:35–48. doi: 10.1016/j.plaphy.2019.09.028
152. Andersson, MS, Saltzman, A, Virk, P, and Pfeiffer, WH. Progress update: crop development of biofortified staple food crops under HarvestPlus. African J Food Agric Nutr Dev. (2017) 17:11905–35. doi: 10.18697/ajfand.78.HarvestPlus05
153. Lepeleire, JD, Strobbe, S, Verstraete, J, Blancquaert, D, and Der Straeten, DV. Folate biofortification of potato by tuber-specific expression of four folate biosynthesis genes. Mol Plant. (2017) 11:175–8. doi: 10.1016/j.molp.2017.12.008
154. Tilocca, MG, Serratrice, G, Oggiano, MA, Mancuso, MR, Mascia, I, Marongiu, E, et al. Monitoring the presence of genetically modified potato EH92-527-1 (BPS-25271-9) in commercial processed food. Ital J Food Saf. (2014) 3:57–9. doi: 10.4081/ijfs.2014.1628
155. Kalia, P, Soi, S, and Muthukumar, P. Marker-assisted introgression of the or gene for enhancing β-carotene content in Indian cauliflower. Acta Hortic. (2016) 1203:121–8.
156. Li, L, and Garvin, DF. Molecular mapping of or, a gene inducing beta-carotene accumulation in cauliflower (Brassica oleracea L. var botrytis). Genome. (2003) 46:588–4. doi: 10.1139/g03-043
157. Sayre, R, Beeching, JR, Cahoon, EB, Egasi, C, Fauquet, C, Fregene, M, et al. The BioCassava plus program: biofortification of cassava for sub-Saharan Africa. Annu Rev Plant Biol. (2011) 62:251–2. doi: 10.1146/annurev-arplant-042110-103751
158. Telengech, PK, Malinga, JN, Nyende, AB, Gichuki, ST, and Wanjala, BW. Gene expression of beta carotene genes in transgenic biofortified cassava. Biotech. (2015) 5:465–2. doi: 10.1007/s13205-014-0243-8
159. Sharma, P, Aggrwal, P, and Kaur, A. Biofrotifcation: a new approach to eradicate hidden hunger. Food Rev Intl. (2017) 33:1–21. doi: 10.1080/87559129.2015.1137309
160. Kim, SH, Kim, YH, Ahn, YO, Ahn, MJ, Jeong, JC, Lee, HS, et al. Downregulation of the lycopene ε-cyclase gene increases carotenoid synthesis via the β-branch-specific pathway and enhances salt-stress tolerance in sweetpotato transgenic calli. Physiol Plant. (2013) 147:432–2. doi: 10.1111/j.1399-3054.2012.01688.x
161. Park, SC, Kim, YH, Kim, SH, Jeong, YJ, Kim, CY, Lee, JS, et al. Overexpression of the IbMYB1 gene in an orange-fleshed sweet potato cultivar produces a dual-pigmented transgenic sweet potato with improved antioxidant activity. Physiol Plant. (2015) 153:525–7. doi: 10.1111/ppl.12281
162. Malik, KA, and Maqbool, A. Transgenic crops for biofortification. Front Sustain Food Syst. (2020) 4:182. doi: 10.3389/fsufs.2020.571402
163. Tumuhimbise, GA, Namutebi, A, Turyashemererwa, F, and Muyonga, J. Provitamin a crops: acceptability, bioavailability, efficacy and effectiveness. Food Nutr Sci. (2013) 4:430–5. doi: 10.4236/fns.2013.44055
164. Szankowski, I, Briviba, K, Fleschhut, J, Schönherr, J, Jacobsen, HJ, and Kiesecker, H. Transformation of apple (Malus domestica Borkh.) with the stilbene synthase gene from grapevine (Vitis vinifera L.) and a PGIP gene from kiwi (Actinidia deliciosa). Plant Cell Rep. (2003) 22:141–9. doi: 10.1007/s00299-003-0668-8185
Keywords: biofortification, hidden hunger, selective breeding, sustainable, vitamins and minerals
Citation: Avnee, Sood S, Chaudhary DR, Jhorar P and Rana RS (2023) Biofortification: an approach to eradicate micronutrient deficiency. Front. Nutr. 10:1233070. doi: 10.3389/fnut.2023.1233070
Edited by:
Monika Thakur, Amity University, IndiaReviewed by:
Saloni Sharma, National Agri-Food Biotechnology Institute, IndiaNeetu Singh, Amity Centre for Biocontrol and Plant Disease Management Amity University Noida U.P, India
Copyright © 2023 Avnee, Sood, Chaudhary, Jhorar and Rana. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Ranbir Singh Rana, cmFuYXJzNjZAZ21haWwuY29t
†ORCID: Avnee, https://orcid.org/0000-0002-5039-8542
Ranbir Singh Rana, https://orcid.org/0000-0003-2038-7479