Abstract
Global population is increasing at an alarming rate which is expected to be around 9.2 billion by 2050 from the present 7.2 billion which urges for higher global crop production to feed world hunger. Cereals and pulses are the two most important crops serving as energy and protein source respectively worldwide. Micronutrients, vitamins, antioxidants, and quality proteins are some of the major areas for crop biofortification in African and Asian countries which is the major caus of annual death of pregnant women and preschool children. Fortification, industrial supplements, dietary variation, and biofortification are the major ways to get rid of these macro- and micronutrient malnutrition. Among them, biofortification is only one of the most viable ways to cater to nutrient-deficient population of the developing countries. Genetic engineering and breeding coupled with agronomic interventions are the only means to take care of this problem. Here, we have summarized the recent progress made in the area of crop biofortification.
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1 Introduction
Using their inbuilt biochemical processes, plants have capabilities to synthesize majority of dietary micronutrients, excluding vitamin D (cholecalciferol, ergocalciferol) and cobalamin (B12) compared to developed nations; crops such as rice, wheat, cassava, and maize are the major sources of energy and proteins in the developing nations which are inadequate to meet the minimum daily requirements of other essential nutrients. Moreover, the nutrients are not evenly distributed in all parts of the plant (Zhu et al. 2007). For instance, rice leaves are rich in provitamin, while the same is lacking in edible grain. Therefore, attention should be given to enrich the dibble portions of the grains with a specific nutrient or combination of more than one by a process commonly known as biofortification.
Biofortified food crops are characterized by enriched nutrients with enhanced bioavailability of essential micronutrients, which are often preferred by the consumers over food supplementation owing to traditional consumption pattern and trade. Biofortification differs from industrial fortification/supplementation as the latter depends upon external addition of micronutrients, whereas the former relies upon changing biosynthesis or physiological capacity of food plants in order to produce or accumulate desired level of specific essential nutrients. The common approaches practiced for generating biofortified crops involve fertilizer application, conventional breeding, and transgenic technology. Implementation of these above-stated approaches results in micronutrient-dense staple crops, with dense minerals and vitamins. Owing to today’s global scenario of increasing nutritional insecurity, biofortification is gaining popularity as it targets the staple food consumed predominantly by the sizeable population inhabiting relatively in the remote areas. Further, developing fortified seeds represents onetime investment which can be consumed year after year and also shared between the communities across the globe (Dwivedi et al. 2012).
Biofortification process pursues various strategies such as optimizing the concentration of antinutrients, mobility of micronutrients within plants, binding capacity/sink strength of seeds, and concentration of metabolites that promote micronutrient absorption (Cakmak et al. 2010). Application of these strategies involves identifying target nutrients suitable for such biofortification. To date, targets for biofortification have been diverted toward essential amino acids (methionine), fatty acids, vitamins A and E, lycopene, flavonoids, Fe, and Zn. In this chapter, we outline the characteristics of the minerals and nutrient elements and evaluate the progress made so far toward enhancement of these targets.
2 Antioxidants
Fruits and vegetables supply passable amount of antioxidants such as anthocyanins, carotenoids, vitamins C and E, and polyphenolics such as quercetin (Shehanaz 2013). These antioxidants protect human from various kinds of reactive oxygen species (ROS). Carotenoids along with other similar compounds are generated via general isoprenoid biosynthetic pathways in plants.
2.1 Anthocyanins
These compounds are colored (red, purple, or blue) pigments that belong to a water-soluble flavonoid family. It has been seen that tomato berry contains negligible amount of anthocyanins. Significant efforts have moderately enhanced its level mainly in peel parts which is normally destroyed during processing. However, the trait of resulting purple fruit was transferred to several commercial cultivars via backcrossing without compromising growth and yield (Hirschi 2008). Further studies have supported the fact that such transgenic tomato powder has extended the life span of tumorigenic mice. Blackberries and raspberries are among the best sources of dietary anthocyanins, but both are expensive and are consumed in smaller quantities than tomatoes (Crozier et al. 2009). Possibly, these engineered tomatoes could contribute substantially to the antioxidant levels of human diets.
2.2 Carotenoids
2.2.1 Lycopene
Lycopene is a carotenoid which is poorly absorbed by the human body from fruits because of its fat-soluble nature. Also, its absorption varies across its cis or trans form. Furthermore, ambiguity prevails concerning the enhanced use of lycopene in foods and its subsequent benefits to human body. Lycopene is the major carotenoid pigment found in tomatoes which has received tremendous attention due to its potential cancer chemopreventive property. Its consumption mostly shields from prostate cancer (Kucuk et al. 2002; Miller et al. 2002). The studies in these lines have produced some inconsistent results, which is soberly clarified by problems with the bioavailability of lycopene from different sources (Giovannucci 2002). Consumption of fruits and vegetables rich in lycopene protects breast and colorectal cancers. While many of the studies conducted on a few animal models have assured a protective reaction of lycopene, its mechanism has been resolved to an appreciable extent (Terry et al. 2002a; Cohen 2002). Heber and Lu (2002) have reported that similar to other dietary carotenoids, lycopene might work in various ways to defend cancer.
Various genetic modification (GM) techniques were used to increase the levels of lycopene in tomato plant. Overexpression of phytoene synthase gene, a key enzyme in the carotenoid pathway from the bacteria Erwinia uredovora in tomato plants, resulted in 1.8- to 2.2-fold enrichment of lycopene and β-carotene and a twofold to fourfold rise in the total carotenoid levels (Fraser et al. 2002). Furthermore, overexpression of a yeast S-adenosyl methionine decarboxylase has increased lycopene levels in tomato fruit significantly (Mehta et al. 2002). Processed tomato such as pastes mixed with fats enhances lycopene absorption significantly. An artificial formulation made by entrapping lycopene within whey proteins was explained in a recent report by Tucker (2003). This lacto-lycopene has shown a similar bioavailability to lycopene in tomato paste (Richelle et al. 2002).
2.3 Vitamin
Biofortification of crops with vitamin A and vitamin C can increase the Fe absorption in the intestine (Garca-Casal et al. 2003). Folate plays a significant role in preventing neuronal disorders in developing fetus. However, it is hard to hold it due to its high water solubility, for example, in rice kernels during boiling (Shrestha et al. 2003). Some of the important biofortified vitamins have been discussed below.
2.3.1 Vitamin A
Rice is a staple food crop of the global population. Overdependence on rice has led to vitamin A deficiency (VAD) which directly affects nearly 250,000–500,000 children every year. Vitamin A-based malnutrition in children can be prevented by improved vitamin A nutrition (Wegmuller et al. 2003). Provitamin A-containing rice could significantly decrease VAD (Zimmermann and Qaim 2004). To decrease the rancidity of rice during storage, oil-rich aleurone layer is removed during milling process, and the remaining endosperm lacks vitamin A. Genetic engineering-based enrichment of rice grain with provitamin A has increased its level significantly (Ye et al. 2000). The immature rice endosperm can produce the intermediate compound geranylgeranyl diphosphate (GGPP) which is then used to generate phytoene by expressing the enzyme phytoene synthase (Cunningham and Gantt 1998). The synthesis of β-carotene from phytoene requires three additional enzymes such as phytoene desaturase, β-carotene desaturase, and lycopene β-cyclase. The important concern is the bioavailability of the engineered β-carotene to humans. Although the conversion factor to vitamin A for synthetic β-carotene and β-carotene in fruits is approximately 6:1, however, the conversion factor in case of vegetables like spinach may be as low as 24:1 due to the poor release of the carotenoids during digestion (Institute of Medicine 2000).
2.3.2 Vitamin E
Another vital dietary antioxidant that occurs in various isomeric forms in plants is vitamin E (tocopherol), with α- and γ-tocopherol being the most abundant. The α-tocopherol is considered as the most beneficial dietary form; however, it is found less dominantly in many foods than γ-tocopherol. Tocochromanols consist of four tocopherols and four tocotrienols that constitute vitamin E (Cahoon et al. 2003; DellaPenna and Pogson 2006). In the plants, vitamin E content can be increased using nutritional genomics (DellaPenna 2007; Shintani and DellaPenna 1998). Furthermore, the content and types of tocochromanols can be altered by coexpression of several genes related to the tocochromanol biosynthetic pathway. This can increase the vitamin E content of seed oil by tenfold (Henry and Qi 2005). Efforts have been made to extend this technology to soybean, maize, and canola (DellaPenna 2007). An added benefit of this work may upsurge the shelf life of foods (Mehta et al. 2002). It is believed that foods with greater levels of vitamin E are protected from oxidative pressure which could enhance agricultural productivity and improve storage.
2.4 Other Antioxidants
Polyphenolics such as flavonols are other important antioxidants which have been enhanced in tomato. In the normal fruit, flavonoids are present in the skin in small amount. Bovy et al. (2002) have increased levels of the kaempferol in a tissue that would normally be lacking this compound in the flesh of the tomato fruit by expression of two transcription factors, LC and C1, from maize.
3 Folate
Folate is also known as tetrahydrofolate (THF) which is not synthesized by animals. The recommended dietary allowance for folate ranges from 400 to 600 μg per day for pregnant women (Rosemary and Lisa 2013). Its deficiency leads to megaloblastic anemia (Scott et al. 2000). Other significances are the initiation of hyperhomocysteinemia which is a risk factor for cardiovascular disease (Stanger 2004), misincorporation of uracil in DNA, and chromosomal damage (Lucock et al. 2003). Furthermore, folate deficiency leads to abnormal DNA methylation arrays associated with carcinogenesis (Choi and Friso 2005; Ulrey et al. 2005). Plants are the ultimate source of folate for animals. Cereals such as maize, wheat, and rice contain extremely low levels of folate (USDA National Nutrient Database for Standard Reference. Release 9; http://www.nal.usda.gov/fnic/foodcomp/search/). To reduce the risk of folate deficiency, fortification of cereal foods with synthetic folic acid has been effected in the USA and other countries (Food and Drug Administration 1996). By contrast, the third world countries lack a solid infrastructural platform to enable effective preventive methods in the form of fortification, supplementation, or educational campaigns (Sachs 2005). Therefore, biofortification of staple crops together with conventional public health practices appears as the probable option to meet the folate deficiency especially in developing countries.
Folate consists of three different components such pteridine, para-aminobenzoic acid (PABA), and glutamate. It is synthesized from these precursors within the mitochondria, while these components are synthesized in unlike compartments within the plant cell (DellaPenna 2007). Bioavailability of folate from various cereals and legume foods depends on a number of factors such as the food matrix, the polyglutamyle conjugation, etc. (McNulty and Pentieva 2004).
The polyglutamylation of folate reduce the bioavailability, because dietary folates need to be deglutamylated by the intestinal conjugase before efficient uptake by intestinal (Rebeille et al. 2006). Recently, it has been exposed that the ratio of monoglutamate to polyglutamate in natural folate derivatives has no clear impact on the intestinal absorption (McKillop et al. 2006). This signifies that the amount of the intestinal conjugase is sufficient to remove the polyglutamate tail without affecting the rate of absorption. This proposes that other factors have an impact on bioavailability, such as entrapment of folates in the food matrix, making them inaccessible to the conjugase that is tethered to the intestinal cell membranes. Therefore, one likely strategy to increase bioavailability could be to boost the levels of the plant conjugase activity of gamma-glutamyl hydrolase (GGH), which would be released from the vacuole following maceration and facilitate folate release within the food matrix before digestion. Other strategy is the use of FBPs. One must also consider the fact that the presence of folate binding proteins (FBPs) in the food matrix, although mechanistically unclear, can lead to a decrease in folate absorption (Witthoft et al. 2006).
4 Essential Amino Acids
Most crops lack one or more essential amino acids, for example, cereal grains are deficient in lysine and threonine, whereas legumes are in methionine and cysteine (Hartwig et al. 1997; Newell-McGloughlin 2008; O’Quinn et al. 2000; Sautter et al. 2006). As the mainstream population of the world depends on cereals and legumes for their diet, plant biologists have used various approaches to augment anticipated deficient amino acids in these plants (Rapp 2002). For example, expression of storage proteins that comprise high levels of required amino acids has raised lysine content in rice and wheat (Christou and Twyman 2004) and some essential amino acid content in potatoes (Egnin and Prakash 1997). However, attempts to raise sulfur-containing amino acids have not been as helpful (Dinkins et al. 2001).
To address this issue, synthetic proteins have been expressed in cassava to match the amino acid requirements for humans. The inadequate availability of free amino acid pools within the edible portion of plants suggests us to alter the amino acid content of target crops. In higher plants, synthesis of threonine, lysine, and methionine are under complex feedback regulation (Hesse et al. 2004). Therefore, studies now focus on developing feedback-insensitive enzymes for these pathways (Newell-McGloughlin 2008). This has significantly improved the free lysine levels in maize (from 2 % to almost 30 %) (Sofi et al. 2009). Expression of these altered enzymes has also improved lysine content in canola and soybean which has significantly improved the production of tryptophan levels in grains. A fundamental concern with each of these manipulations is to ensure that the total amount and composition of storage proteins are not changed.
5 Essential and Very-Long-Chain Fatty Acids
Genetically modified oil seed crops are an abundant, relatively inexpensive source of dietary fatty acids (Abbadi et al. 2004; Anai et al. 2003; Kinney and Knowlton 1998; Liu et al. 2002; Reddy and Thomas 1996; Wallis et al. 2002). Production of these lipids in vegetables could provide an easy mechanism to deliver healthier products without major dietary modifications (Damude and Kinney 2008; Newell-McGloughlin 2008). Plants are sources of the essential fatty acids such as linoleic acid and linolenic acid as well as very-long-chain polyunsaturated fatty acids (VLC-PUFAs) such as arachidonic acid (ARA), eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA), which are usually found in fish oils.
Given that many of the enzymes tangled in fatty acid biosynthesis and degradation have been characterized, there is an abundance of transgenic approaches to the modification of oil and fat content in plants (Damude and Kinney 2008; Broun et al. 1999). Examples of such modified oils include low- and zero-saturated fat soybean and canola oils, canola oil comprising medium-chain fatty acids, high-stearic acid canola oil, high-oleic acid soybean oil, and canola oil encompassing the polyunsaturated fatty acid linolenic acid (Mensink et al. 2003). Oils abundant in monounsaturated fatty acids provide improved oil stability, flavor, and nutritional qualities. Oleic acid (18:1), a MUFA, can provide more stability and health benefits than the PUFA (18:2 and 18:3). Soybeans have been manipulated to encompass more than 80 % oleic acid against normal 23 % and had a significant decrease in polyunsaturated fatty acids (Kinney and Knowlton 1998). High-oleic acid soybean oil is more resistant to degradation by heat and oxidation requiring little or no post-refining processing.
6 Mineral Biofortification
Humans require at least 22 mineral elements for their survivals (Welch and Graham 2004; White and Broadley 2005; Graham et al. 2007) which can be abounding by an appropriate diet. It is estimated that over 60 % of the world’s people are iron (Fe) deficient, over 30 % are zinc (Zn) deficient, 30 % are iodine (I) deficient, and 15 % are selenium (Se) deficient (Yang et al. 2007). In addition, calcium (Ca), magnesium (Mg), and copper (Cu) deficiencies are also common in many developed and developing countries (Frossard et al. 2000; Welch and Graham 2002, 2005; Rude and Gruber 2004; Grusak and Cakmak 2005; Thacher et al. 2006).
Fe is an essential component of many enzymes catalyzing redox reactions. More than half of the Fe in the human body is bound to hemoglobin. In the developing countries, Fe deficiency leads to anemia and is estimated that 40–45 % of preschool-age children are anemic. Approximately 50 % of this anemia results from Fe deficiency (Grillet et al. 2014). The significances of early childhood anemia include poor cognitive development (Lozoff 2007). Zn is a cofactor with diverse structural and catalytic functions in about 10 % of all human proteins. In addition, evidence has been accumulating for important regulatory roles of Zn ions in inter- and intracellular signaling (Maret 2013). A major challenge is low bioavailability of Fe and Zn from staple cereals and legumes which have absorption inhibitor such as phytic acid (Olsen and Palmgren 2014). In general, to increase mineral concentrations in edible crops (biofortification), parallel attempts are advocated such as (1) to increase the concentrations of “promoter” substances, such as ascorbate (vitamin C), β-carotene, cysteine-rich polypeptides, and certain organic and amino acids, which excite the absorption of essential mineral by the gut; (2) to reduce the concentrations of antinutrients, such as oxalate, polyphenolics (tannins), or phytate (IP6), which interfere with their absorption; (3) and to increase the mobility of Fe and Zn within the plant as well as the binding capacity/sink strength of seeds.
A recent study reported the absorption of radio-labeled Zn from maize, rice, and barley with low phytic acid mutants in comparison to cultivars with normal seed phytate concentrations. Consistently, reduced phytic acid levels resulted in enhanced Zn absorption (Lonnerdal et al. 2011). In the rice, bioavailability of iron has been targeted by introducing a gene for phytase which resulted in a 130-fold increase in the expression of this enzyme. On the other hand, dietary phytate has been associated with substantial health benefits including strong activity as an anticarcinogenic agent. Several studies reported inhibitory effects of phytate on the growth of different types of tumors. Additional protective effects include the lowering of cholesterol levels (Vucenik and Shamsuddin 2006). Thus, the nutritional benefits of low-phytate grains and seeds have to be weighed against the positive effects of phytate intake (Murgia et al. 2012). The conclusions drawn could well differ between populations depending on the relative importance of micronutrient malnutrition versus cancer incidence.
Transgenic maize plants overexpressing ferritin in combination with a fungal phytase contained up to threefold more bioavailable Fe as determined by the in vitro digestion/Caco-2 system (Drakakaki et al. 2005). Expression of ferritin, an iron-storage protein, in seeds causes a threefold to fourfold increase in iron levels (Goto et al. 2000, 1999; Vasconcelos et al. 2003). Although polishing of rice causes a decrease in mineral levels, ferritin-enhanced rice still has increased iron levels in the transgenic polished rice. Rats fed with a diet containing the transgenic rice demonstrate that the iron in the rice had bioavailability equal to that found in diets containing FeSO4 at equal concentrations (Murray-Kolb et al. 2002).
A potentially promising alternative approach was suggested to indirectly enhance Fe and Zn bioavailability through increasing the concentration of nondigestible carbohydrates, thereby promoting beneficial microbiota that stimulates Fe and Zn absorption by human gut cells (Murgia et al. 2012; Shahzad et al. 2014). The main focus has been on inulin, a polymer consisting of beta-2-1-linked fructose units. Supplemented inulin had enhanced bioavailability of Fe in maize and soybean meals (Yasuda et al. 2006). Variation in concentrations among crop plants and engineering strategies has to be explored more extensively for this prebiotic (Rawat et al. 2013). A combined approach in rice and maize has been developed that involves the expression of iron-storage proteins and fungal phytase (Bashir et al. 2013). This combined approach for mineral biofortification should provide maximal levels of bioavailable iron.
7 Conclusions
In conclusion, with the increasing global population and nutritional insecurity mainly in developing nations, research priorities should be redefined and reoriented to a more meaningful approach to solve the problem. Combined approach of genetic engineering, breeding, and agronomic intervention could help figure out above nutritional problem. Future research should be diverted to analyze the interaction of augmented nutrients with other nutrients in vivo. It is also advised that the impact of genetic engineering on the agronomic performance of crops and biotic and abiotic stresses should also be assessed. In addition, the focus should be on studies involving field crop trials and human beings as experimental subjects to analyze the effectiveness of agronomic or genetic biofortification.
References
Abbadi A, Domergue F, Bauer J, Napier JA, Welti R, Zahringer U, Cirpus P, Heinz E (2004) Biosynthesis of very-long-chain polyunsaturated fatty acids in transgenic oilseeds: constraints on their accumulation. Plant Cell 16:2734–2748
Anai T, Koga M, Tanaka H, Kinoshita T, Rahman SM, Takagi Y (2003) Improvement of rice (Oryza sativa L.) seed oil quality through introduction of a soybean microsomal omega-3 fatty acid desaturase gene. Plant Cell Rep 21:988–992
Bashir K, Takahashi R, Nakanishi H, Nishizawa NK (2013) The road to micronutrient biofortification of rice: progress and prospects. Front Plant Sci 4:1–7
Bovy A, de Vos R, Kemper M, Schijlen E, Pertejo MA, Muir S, Collins G, Robinson S, Verhoeyen M, Hughes S, Santos BC, van Tunen A (2002) High-flavonol tomatoes resulting from the heterologous expression of the maize transcription factor genes LC and C1. Plant Cell 10:2509–2526
Broun P, Gettner S, Somerville C (1999) Genetic engineering of plant lipids. Annu Rev Nutr 19:197–216
Cahoon EB, Hall SE, Ripp KG, Ganzke TS, Hitz WD, Coughlan SJ (2003) Metabolic redesign of vitamin E biosynthesis in plants for tocotrienol production and increased antioxidant content. Nat Biotechnol 21:1082–1087
Cakmak I, Pfeiffer WH, McClafferty B (2010) Review: biofortification of durum wheat with zinc and iron. Cereal Chem 87:10–20
Choi SW, Friso S (2005) Interactions between folate and aging for carcinogenesis. Clin Chem Lab Med 43:1151–1157
Christou P, Twyman RM (2004) The potential of genetically enhanced plants to address food insecurity. Nutr Res Rev 17:23–42
Cohen LA (2002) A review of animal model studies of tomato carotenoids, lycopene, and cancer chemoprevention. Exp Biol Med 227:864–868
Crozier A, Jaganath IB, Clifford MN (2009) Review article dietary phenolics: chemistry, bioavailability and effects on health. Nat Prod Rep 26:1001–1043
Cunningham FX, Gantt G (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant MolBiol 49:557–583
Damude HG, Kinney AJ (2008) Enhancing plant seed oils for human nutrition. Plant Physiol 147:962–968
DellaPenna D (2007) Biofortification of plant-based food: enhancing folate levels by metabolic engineering. Proc Natl Acad Sci U S A 104:3675–3676
DellaPenna D, Pogson BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–738
Dinkins RD, Reddy MSS, Meurer CA, Yan B, Trick H, Thibaud-Nissen F, Finer JJ, Wayne A, Parrott WA, Collins GB (2001) Increased sulfur amino acids in soybean plants over expressing the maize 15 kDa zein protein. In Vitro Cell Dev Biol Plant 37:742–747
Drakakaki G, Marcel S, Glahn RP, Lund EK, Pariagh S, Fischer R, Christou P, Stoger E (2005) Endosperm-specific co-expression of recombinant soybean ferritin and Aspergillus phytase in maize results in significant increases in the levels of bioavailable iron. Plant Mol Biol 59:869–880
Dwivedi SL, Sahrawat KL, Rai KN, Blair MW, Andersson MS, Pfeiffer W (2012) Nutritionally enhanced staple food crops. Plant Breed Rev 36:169–292
Egnin M, Prakash CS (1997) Transgenic sweet potato expressing a synthetic storage protein gene exhibits high level of total protein and essential amino acids. In Vitro Cell Dev Biol Plant 33:52A
Food and Drug Administration (1996) Food standards: amendment of standards of identity for enriched grain products to require addition of folic acid. Final rule, 21 CFR parts 136, 137, 139:8781–8807
Fraser PD, Romer S, Shipton CA, Mills PB, Kiano JW, Misawa N, Drake RG, Schuch W, Bramley PM (2002) Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc Natl Acad Sci USA 99:1092–1097
Frossard E, Bucher M, Machler F, Mozafar A, Hurrell R (2000) Potential for increasing the content and bioavailability of Fe, Zn and Ca in plants for human nutrition. J Sci Food Agric 80:861–879
Garca-Casal MN, Layrisse M, Pena-Rosas JP, Ramrez J, Leets I, Matus P (2003) Iron absorption from elemental iron-fortified cornflakes in humans. Role of vitamins A and C1-3. Nutr Res 23:451–463
Giovannucci E (2002) Lycopene and prostate cancer risk. Methodological considerations in the epidemiologic literature. Pure Appl Chem 74:1427–1434
Goto F, Yoshihara T, Shigemoto N, Toki S, Takaiwa F (1999) Iron fortification of rice seed by the soybean ferritin gene. Nat Biotechnol 17:282–286
Goto F, Yoshihara T, Saiki H (2000) Iron accumulation and enhanced growth in transgenic lettuce plants expressing the iron-binding protein ferritin. Theor Appl Genet 100:658–664
Graham RD, Welch RM, Saunders DA, Ortiz-Monasterio I, Bouis HE, Bonierbale M, de Haan S, Burgos G, Thiele G, Liria R, Craig A, Meisner CA, Beebe SE, Potts MJ, Kadian M, Hobbs PR, Gupta RK, Twomlow S (2007) Nutritious subsistence food systems. Adv Agron 92:1–74
Grillet L, Mari S, Schmidt W (2014) Iron in seeds–loading pathways and subcellular localization. Front Plant Sci 4:535
Grusak MA, Cakmak I (2005) Methods to improve the crop-delivery of minerals to humans and livestock. In: Broadley MR, White PJ (eds) Plant nutritional genomics. Blackwell, Oxford, pp 265–286
Hartwig EE, Kuo TM, Kenty MM (1997) Seed protein and its relationship to soluble sugars in soybeans. Crop Sci 37:770–773
Heber D, Lu QY (2002) Overview of mechanisms of action of lycopene. Exp Biol Med 227:920–923
Henry EV, Qi Q (2005) Biotechnological production and application of vitamin E: current state and prospects. Appl Microbiol Biotechnol 68:436–444
Hesse H, Kreft O, Maimann S, Zeh M, Hoefgen R (2004) Current understanding of the regulation of methionine biosynthesis in plants. J Exp Bot 55:1799–1808
Hirschi KD (2008) Nutritional improvements in plants: time to bite on biofortified foods. Trends Plant Sci 13:459–514
Institute of Medicine (2000) Carotene and other carotenoids. In: Dietary reference intakes for vitamin C, vitamin E, selenium, and carotenoids. National Academy Press, Washington, DC, pp 325–382
Kinney AJ, Knowlton S (1998) Designer oils: the high oleic acid soybean. In: Roller S, Harlanders S (eds) Genetic modification in the food industry: a strategy for food quality improvement. Blackie Academic and Professional/Thomson Science, London, pp 193–213
Kucuk O, Sarkar FH, Sakr W, Khachik F, Djuric Z, Banerjee M, Pollak MN, Bertram JS, Wood DP (2002) Lycopene in the treatment of prostate cancer. Pure Appl Chem 74:1443–1450
Liu Q, Singh S, Green A (2002) High-oleic and high-stearic cottonseed oils: nutritionally improved cooking oils developed using gene silencing. J Am Coll Nutr 21:205S–211S
Lonnerdal B, Mendoza C, Brown KH, Rutger JN, Raboy V (2011) Zinc absorption from low phytic acid genotypes of maize (Zea mays L.), barley (Hordeum vulgare L.), and rice (Oryza sativa L.) assessed in a suckling rat pup model. J Agric Food Chem 59:4755–4762
Lozoff B (2007) Iron deficiency and child development. Food Nutr Bull 28:S560–S571
Lucock M, Yatesa Z, Glanvillea T, Leemingc R, Simpsona N, Daskalakisd I (2003) A critical role for B-vitamin nutrition in human developmental and evolutionary biology. Nutr Res 23:1463–1475
Maret W (2013) Zinc biochemistry: from a single zinc enzyme to a key element of life. Adv Nutr 4:82–91
McKillop DJ, McNulty H, Scott JM, McPartlin JM, Strain JJ, Bradbury I, Girvan J, Hoey L, McCreedy R, Alexander J, Patterson BK, Hannon-Fletcher M, Pentieva K (2006) The rate of intestinal absorption of natural food folates is not related to the extent of folate conjugations. Am J Clin Nutr 84:167–173
McNulty H, Pentieva K (2004) Folate bioavailability. Proc Nutr Soc 63:529–536
Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002) Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life. Nat Biotechnol 20:613–618
Mensink RP, Zock PL, Kester DM, Katan MB (2003) Effects of dietary fatty acids and carbohydrates on the ratio of serum total to HDL cholesterol and on serum lipids and apolipoproteins: a meta-analysis of 60 controlled trials. Am J Clin Nutr 77:1146–1155
Miller EC, Hadley CW, Schwartz SJ, Erdman JW, Boileau TWM, Clinton SK (2002) Lycopene, tomato products, and prostate cancer prevention. Have we established causality? Pure Appl Chem 74:1435–1441
Murgia I, Arosio P, Tarantino D, Soave C (2012) Biofortification for combating hidden hunger for iron. Trends Plant Sci 17:47–55
Murray-Kolb LE, Takaiwa F, Goto F, Yoshihara T, Theil EC, Beard JL (2002) Transgenic rice is a source of iron for iron-depleted rats. J Nutr 132:957–960
Newell-McGloughlin M (2008) Nutritionally improved agricultural crops. Plant Physiol 147:939–953
O’Quinn PR, Nelssen JL, Goodband RD, Knabe DA, Woodworth JC, Tokach MD, Lohrmann TT (2000) Nutritional value of a genetically improved high-lysine, high-oil corn for young pigs. J Anim Sci 78:2144–2149
Olsen LI, Palmgren MG (2014) Many rivers to cross: the journey of zinc from soil to seed. Front Plant Sci 5:30
Rapp W (2002) Development of soybeans with improved amino acid composition. In: 93rd AOCS annual meeting and expo. Montreal/Champaign, Journal of the American Oil Chemists' Society, pp 79–86
Rawat N, Neelam K, Tiwari VK, Dhaliwal HS (2013) Biofortification of cereals to overcome hidden hunger. Plant Breed 132:437–445
Rebeille F, Ravanel S, Jabrin S, Douce R, Storozhenko S, Straeten DVD (2006) Folates in plants: biosynthesis, distribution, an enhancement. Physiol Plant 126:330–342
Reddy AS, Thomas TL (1996) Expression of a cyanobacterial DELTA 6-desaturase gene results in gamma-linolenic acid production in transgenic plants. Nat Biotechnol 14:639–642
Richelle M, Bortlik K, Liardet S, Hager C, Lambelet P, Baur M, Applegate LA, Offord EA (2002) A food-based formulation provides lycopene with the same bioavailability to humans as that from tomato paste. J Nutr 132:404–408
Rosemary AS, Lisa AH (2013) Nutrient Intake values for folate during pregnancy and lactation vary widely around the world. Nutrients 5:3920–3947
Rude RK, Gruber HE (2004) Magnesium deficiency and osteoporosis: animal and human observations. J Nutr Biochem 15:710–716
Sachs JD (2005) Millennium project investing in development: a practical plan to achieve the millennium development goals. First published by Earthscan in the UK and USA
Sautter C, Poletti S, Zhang P, Gruissem W (2006) Biofortification of essential nutritional compounds and trace elements in rice and cassava. Proc Nutr Soc 65:153–159
Scott J, Rebeill F, Fletcher J (2000) Folic acid and folates: the feasibility for nutritional enhancement in plant foods. J Sci Food Agric 80:795–824
Shahzad Z, Rouached H, Rakha A (2014) Combating mineral malnutrition through iron and zinc biofortification of cereals. Compr Rev Food Sci Food Saf 13:329–346
Shehanaz A (2013) The antioxidant effect of certain fruits. Int J Pharm Sci Res 5(12):265–268
Shintani D, DellaPenna D (1998) Elevating the vitamin E content of plants through metabolic engineering. Science 282:2098–2100
Shrestha AK, Arcot J, Paterson JL (2003) Edible coating materials-their properties and use in the fortification of rice with folic acid. Food Res Int 36:921–928
Sofi PA, Wani SA, Rather AG, Wani SH (2009) Quality protein maize (QPM): genetic manipulation for the nutritional fortification of maize. J Plant Breed Crop Sci 6:244–253
Stanger O (2004) The potential role of homocysteine in percutaneous coronary interventions (PCI): review of current evidence and plausibility of action. Cell Mol Biol 50:953–988
Terry P, Jain M, Miller AB, Howe GR, Rohan TE (2002a) Dietary carotenoids and risk of breast cancer. Am J Clin Nutr 76:883–888
Terry P, Jain M, Miller AB, Howe GR, Rohan TE (2002b) Dietary carotenoid intake and colorectal cancer risk. Nutr Cancer 42:167–172
Thacher TD, Fischer PR, Strand MA, Pettifor JM (2006) Nutritional rickets around the world: causes and future directions. Ann Trop Paediatr 26:1–16
Tucker G (2003) Nutritional enhancement of plants. Curr Opin Biotechnol 14:221–225
Ulrey CL, Liu L, Andrews LG, Tollefsbol TO (2005) The impact of metabolism on DNA methylation. Hum Mol Genet 14:R139–R147
Vasconcelos M, Datta K, Oliva N, Khalekuzzaman M, Torrizo L, Krishnan S, Oliveira M, Goto F, Datta SK (2003) Enhanced iron and zinc accumulation in transgenic rice with the ferritin gene. Plant Sci 164:371–378
Vucenik I, Shamsuddin AM (2006) Protection against cancer by dietary IP6 and inositol. Nutr Cancer 55:109–125
Wallis JG, Watts JL, Browse J (2002) Polyunsaturated fatty acid synthesis: what will they think of next? Trends Biochem Sci 27:467–473
Wegmuller R, Zimmermann MB, Hurrell RF (2003) Dual fortification of salt with iodine and encapsulated iron compounds: stability and acceptability testing in Morocco and Cote d’Ivoire. J Food Sci 68:2129–2135
Welch RM, Graham RD (2002) Breeding crops for enhanced micronutrient content. Plant Soil 245:205–214
Welch RM, Graham RD (2004) Breeding for micronutrients in staple food crops from a human nutrition perspective. J Exp Bot 55:353–364
Welch RM, Graham RD (2005) Agriculture: the real nexus for enhancing bioavailable micronutrients in food crops. J Trace Elem Med Biol 18:299–307
White PJ, Broadley MR (2005) Biofortifying crops with essential mineral elements. Trends Plant Sci 10:586–593
Witthoft CM, Arkbage K, Johansson M, Lundin E, Berglund G, Zhang JX, Lennernas H, Dainty JR (2006) Folate absorption from folate-fortified and processed foods using a human ileostomy model. Br J Nutr 95:181–187
Yang XE, Chen WR, Feng Y (2007) Improving human micronutrient nutrition through biofortification in the soil–plant system: China as a case study. Environ Geochem Health 29:413–428
Yasuda K, Roneker KR, Miller DD, Welch RM, Lei XG (2006) Supplemental dietary inulin affects the bioavailability of iron in corn and soybean meal to young pigs. J Nutr 136:3033–3038
Ye X, Al-Babili S, Kloti A, Zhang J, Lucca P, Beyer P, Potroykus I (2000) Engineering the provitamin A (beta-carotene) biosynthetic pathway into (carotenoid-free) rice endosperm. Science 287:303–305
Zhu C, Naqvi S, Gomez-Galera S, Pelacho AM, Capell T, Christou P (2007) Transgenic strategies for the nutritional enhancement of plants. Trends Plant Sci 12:548–555
Zimmermann R, Qaim M (2004) Potential health benefits of golden rice: a Philippine case study. Food Policy 29:147–168
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Meena, N.L., Gupta, O.P., Sharma, S.K. (2016). Nutritional Enhancers/Promoters in Biofortification. In: Singh, U., Praharaj, C., Singh, S., Singh, N. (eds) Biofortification of Food Crops. Springer, New Delhi. https://doi.org/10.1007/978-81-322-2716-8_25
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