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Biofortification: Introduction, Approaches, Limitations, and Challenges

Chapter · January 2016

DOI: 10.1007/978-81-322-2716-8_1

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 Biofortification: Introduction, Approaches,
Limitations, and Challenges 1
Ummed Singh, C S Praharaj, S.K. Chaturvedi,
and Abhishek Bohra

Abstract
Micronutrient malnutrition is known to affect more than half of the
world’s population and considered to be among the most serious global
challenges to humankind. Modern plant breeding has been historically
oriented toward achieving high agronomic yields rather than nutritional
quality, and other efforts related to alleviating the problem have been
primarily through industrial fortification or pharmaceutical supplementa-
tion. Micronutrient malnutrition or the hidden hunger is very common
among women and preschool children caused mainly by low dietary
intake of micronutrients, especially Zn and Fe. Biofortification, the pro-
cess of increasing the bioavailable concentrations of essential elements in
edible portions of crop plants through agronomic intervention or genetic
selection, may be the solution to malnutrition or hidden hunger mitigation.
The Consultative Group on International Agricultural Research has been
investigating the genetic potential to increase bioavailable Fe and Zn in
staple food crops such as rice, wheat, maize, common beans, and cassava.

Keywords
Biofortification • Breeding • Genetic engineering • Limitations • Strategy

1.1 Introduction
U. Singh (*) • C S Praharaj
Division of Crop Production, ICAR-Indian Institute of Biofortification, the process of breeding nutrients
Pulses Research, Kanpur, Uttar Pradesh 208 024, India into food crops, provides a comparatively cost-
e-mail: [email protected]; cspraharaj@hotmail. effective, sustainable, and long-term means of
com delivering more micronutrients. This approach
S.K. Chaturvedi • A. Bohra not only will lower the number of severely mal-
Division of Crop Improvement, ICAR-Indian Institute of nourished people who require treatment by com-
Pulses Research, Kanpur, Uttar Pradesh 208 024, India
e-mail: [email protected]; plementary interventions but also will help them
[email protected] maintain improved nutritional status. Moreover,

# Springer India 2016 3

U. Singh et al. (eds.), Biofortification of Food Crops, DOI 10.1007/978-81-322-2716-8_1

[email protected]
4 U. Singh et al.

biofortification provides a feasible means of 1.2.1 Iodine

reaching malnourished rural populations who
may have limited access to commercially Iodine is an essential component of the thyroid
marketed fortified foods and supplements. hormones thyroxine and triiodothyronine, which
The biofortification strategy seeks to put the regulate growth and development and maintain
micronutrient-dense trait in those varieties that the basal metabolic rate. However, only 30 % of
already have preferred agronomic and consump- the body’s iodine is stored in the thyroid gland,
tion traits, such as high yield. Marketed surpluses and the precise role of the 70 % distributed in
of these crops may make their way into retail other tissues is unknown. It may overlap with the
outlets, reaching consumers in first rural and function of other minerals such as Se or Fe and
then urban areas, in contrast to complementary Zn (Lyons et al. 2004). Goiter is another impor-
interventions, such as fortification and supple- tant symptom of iodine deficiency and results
mentation, that begin in urban centers. from the lack of thyroxine inducing the produc-
Biofortified staple foods cannot deliver as high tion of thyroid-stimulating hormone, which in
a level of minerals and vitamins per day as turn causes the thyroid gland to swell (Dunn
supplements or industrially fortified foods, but 2003). India is one of the worst affected countries
they can help by increasing the daily adequacy in the world, with more than 50 million cases of
of micronutrient intakes among individuals goiter and more than two million of cretinism.
throughout the life cycle (Bouis et al. 2011).

1.2.2 Vitamin A
1.2 Minerals and Vitamins
Deficiency associated with blindness and
Minerals, in the context of the human diet, are increased risk of disease and death for small
inorganic chemical elements (or more properly children and pregnant women can be addressed
their dissociated ions) that are required for through supplements, which are now estimated
biological or biochemical processes including to reach children at least once a year in
the accumulation of electrolytes. Carbon, hydro- 40 countries. The UN Standing Committee on
gen, nitrogen, and oxygen are excluded from the Nutrition (UN/SCN) estimates that 140 million
list as these are found in common organic children and 7 million pregnant women are VA
molecules. There are 16 essential minerals, but deficient, primarily in Africa and South/South-
11 of them are required in such small amounts east Asia. In 1998, WHO, UNICEF, Canadian
and/or are so abundant in food and drinking International Development Agency, USAID,
water that deficiency arises only in very unusual and the Micronutrient Initiative launched the
circumstances. The remaining five are present in VA Global Initiative. This provides support to
limiting amounts in many foods, so a monoto- countries in delivering VA supplements.
nous diet can easily result in deficiency. These
minerals are iodine (I), iron (Fe), zinc (Zn), cal-
cium (Ca), and selenium (Se). Deficiency 1.2.3 Iron
diseases arise when diets are based predomi-
nantly on staple foods, such as milled cereals, Iron has numerous important functions in the
which have a low bioavailable mineral content human body, reflecting its ability to act as both
(Christou and Twyman 2004). Mineral defi- an electron donor and acceptor. In this role, it
ciency is therefore most prevalent in developing forms the functional core of the heme complex,
countries, where there is poor access to fresh which is found in the oxygen-binding molecules
foods, although Ca deficiency is also widespread hemoglobin and myoglobin, and the catalytic
in the industrialized world (Galera et al. 2010). center of cytochromes, which carry out redox

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1 Biofortification: Introduction, Approaches, Limitations, and Challenges 5

reactions. Iron is therefore required for oxygen signaling molecule (a secondary messenger). It
transport in the body and for energy metabolism, plays a pivotal role in the blood clotting cascade.
also contributing to the catalytic activity of a Calcium deficiency has a profound impact on
range of nonheme enzymes such as ribonuclease bone health, resulting in rickets if deficiency
reductase (WHO/FAO 1998). The immediate occurs in the young and osteoporosis if it persists
outcome of Fe deficiency is iron deficiency ane- into old age.
mia (IDA), which is thought to affect at least two
billion people worldwide. More than half of these
cases could be addressed by increasing the 1.2.6 Selenium
amount of Fe in the diet, but as for iodine this
is difficult in developing countries where the Selenium is found in two unusual amino acids—
population relies on staples, because cereal selenocysteine and selenomethionine—which
grains contain very low levels of Fe and also are the principal functional components of
contain antinutritional compounds such as selenoenzymes. It is an essential cofactor in
phytate that inhibit Fe uptake (Zimmermann approximately 50 enzymes, including those
et al. 2004). whose function is to reduce antioxidant enzymes
(such as glutathione peroxidase) and those whose
function is to remove mineral ions from other
1.2.4 Zinc proteins (such as thyroid hormone deiodinases)
(Lyons et al. 2004). Se is an antioxidant with
Zinc is an essential functional component of health benefits including the prevention of cancer
thousands of proteins. Many contain zinc pros- and heart disease (WHO/FAO 1998).
thetic groups (e.g., zinc finger, zinc twist) and
approximately 100 enzymes require Zn as a
cofactor. Some olfactory receptors cannot func- 1.2.7 Folate
tion without Zn. Many cells in the body also
secrete Zn as a signaling molecule, including Deficiency associated with increased risk of
cells in the immune and nervous systems maternal death and complications in birth and
(WHO/FAO 1998). Nearly two billion people also associated with neural tube defects in infants
are at risk of Zn deficiency, predominantly chil- and with an estimated 200,000 severe birth defects
dren and pregnant women. Signs of severe zinc every year can be addressed through fortification
deficiency include hair loss, skin lesions, of wheat products (Haddad et al. 2004).
wasting, and persistent diarrhea. The mineral
appears to be particularly important during
periods of rapid growth, and insufficient intake 1.3 Alleviating Hidden Hunger:
during childhood and adolescence can delay Interventions
growth, sexual development, and psychomotor
development (WHO/FAO 1998). The term “hidden hunger” has been used to
describe the micronutrient malnutrition inherent
in human diets that are adequate in calories but
1.2.5 Calcium lack vitamins and/or mineral elements. The diets
of a large proportion of the world’s population
Calcium is the most abundant mineral in the are deficient in Fe, Zn, Ca, Mg, Cu, Se, or I,
human body, accounting for 1–2 % of an adult’s which affects human health and longevity and
body mass. Over 99 % of Ca is stored in the teeth therefore national economies. Mineral malnutri-
and bones, where it plays an important structural tion can be addressed by increasing the amount
role (WHO/FAO 1998). However, Ca, like Zn, is of fish and animal products in diets, mineral
also an enzyme cofactor and an important supplementation, and food fortification and/or

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6 U. Singh et al.

increasing the bioavailability of mineral Zinc fortification has been implemented in the
elements in edible crops. However, strategies to industrial world but rarely in developing
increase dietary diversification, mineral supple- countries. One exception is Zn-fortified wheat
mentation, and food fortification have not always and maize flours in Mexico, which are used to
proved successful. For this reason, the bioforti- make bread and tortillas, the two principal
fication of crops through the application of min- staples (IZINCG 2007). Organizations such as
eral fertilizers, combined with breeding varieties the Zinc Task Force (ZTF) and the International
with an increased ability to acquire mineral Zinc Nutrition Consultative Group (IZiNCG) are
elements, has been advocated (White and fighting Zn malnutrition by promoting diverse
Broadley 2009). strategies to eliminate it. As Zn and Fe
Food fortification and supplementation are cur- deficiencies tend to go hand in hand, it has been
rently the most cost-effective strategies to address suggested that double fortification would be
global mineral malnutrition. The most successful effective with little additional cost, particularly
strategy has been salt iodization (fortification with if Fe fortification were already in place.
iodine) which has reduced the incidence of goiter
and other IDD symptoms markedly where the
scheme has been introduced (Galera et al. 2010). 1.3.2 Industrial Fortification
Most strategies to improve mineral nutrition have
been less successful because of political, socio- The marketed supply of a widely consumed sta-
economic, infrastructure-related, and technical ple food can be fortified by adding
constraints that are apparent in most developing micronutrients at the processing stage, and his-
countries. torically this is how micronutrient deficiencies
have been addressed in the developed world.
Concentration in the food industry also tends to
strengthen compliance and quality assurance.
1.3.1 Food Fortification Consumption of wheat flour products is growing
around the world, even where wheat is not a
Food fortification is one of the most cost- traditional food staple, opening new fortification
effective long-term strategies for mineral nutri- opportunities at the milling stage. Public support
tion (Horton 2006). Fortification of dairy for traditional fortification has recently been
products such as bread and milk with different enhanced by new promotion and coordination
minerals (and vitamins) has been successful in efforts: Micronutrient Initiative (based in
industrialized countries However, this strategy is Canada), Flour Fortification Initiative (based in
difficult to implement in developing countries Emory University), Mid Day Meal Scheme
because it relies on a strong food processing (India), and the Global Alliance for Improved
and distribution infrastructure. Fortification Nutrition (GAIN, based in Geneva). Other
takes place during food processing and increases important global actors include the Network for
the product price. These factors make fortified Sustained Elimination of Iodine Deficiency and
products unaffordable to the most impoverished the International Zinc Nutrition Consultative
people living in remote rural areas. Since many Group. In addition, efforts are underway to set
parts of the world suffer from multiple regional standards for fortification. The Flour
deficiencies, strategies must also be developed Fortification Initiative provides an assessment
to fortify foods simultaneously with several of global progress, and they report that 26 % of
micronutrients without adverse interactions the global wheat market is fortified, benefiting
among them (Zimmermann et al. 2004). The 1.8 billion people. Most wheat fortification
addition of a single micronutrient would have efforts in the developing world are still prelimi-
more or less the same cost implications as the nary or on a pilot scale; they are primarily in
addition of several (Alavi et al. 2008). the Western Hemisphere, with little sustained

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1 Biofortification: Introduction, Approaches, Limitations, and Challenges 7

activity in Asia and Africa, where most of the Schultink 2002). In industrialized countries, with
micronutrient deficient populations live. Certain few mineral malnutrition problems, supplementa-
kinds of fortification may be impractical for tion is focused on a small subset of the population
some important food staples (e.g., VA fortifica- with specific deficiencies resulting from medical
tion of milled rice) or may introduce off colors or conditions. In developing countries, where acute
flavors (e.g., VA fortification of white maize). and chronic deficiencies are common, supplemen-
Industrial fortification will only apply to tation is highly recommended to complement the
marketed supplies and therefore may not reach diet (fortified or otherwise) of the entire popula-
those among the poor who obtain food outside of tion (Nantel and Tontisirin 2002).
commercialized channels. Given these Periodic provision of supplements (often in the
limitations, it is clear that industrial fortification form of tablets) can address deficiencies of
of food cannot provide a complete solution to the micronutrients that are stored in the body, such
problem of micronutrient deficiencies in the as vitamin A and iron. Supplementation can be
medium term. It is in this context that a role cheap compared to the large public health benefit.
emerges for biofortification as a complementary The total annual cost of iron tablet supplementa-
strategy. tion in India to reach 27 million women and
128 million children at risk is only $5.2 million.
Yet even small budgets can be difficult to sustain
1.3.3 Promotion of Dietary year after year when they are dedicated to the
Diversification welfare of politically weak or socially marginal
beneficiaries. Furthermore, while certain
Education is an important element in ensuring populations are easy to reach through existing
that improvements in income result in better institutions (e.g., schoolchildren through schools),
maternal and child health. However, dietary it is often difficult to accomplish full coverage of
diversification is constrained by resource avail- those most at risk—poor women and very young
ability for poor households and seasonal avail- children. Thus, supplementation has often been
ability of fruits and vegetables. Promotion of most effective when delivered together with
home gardens is often touted, but the poor have other maternal and child health interventions.
a high opportunity cost for their labor and often The distribution of vitamin A supplements has
limited land. Increased production of fruits and been one of the most cost effective and success-
vegetables for household use reduces resources ful acute intervention programs in the developing
available for other income-earning or food pro- world (Shrimpton and Schultink 2002), but this is
duction activities. This type of effort is also rela- a rarity. Like fortification, successful supplemen-
tively expensive and difficult to sustain on any tation strategies require a robust infrastructure
large scale. and a government determined to improve the
nutritional health of its population (Shrimpton
and Schultink 2002). Even more than fortifica-
1.3.4 Food Supplementation tion, supplementation requires compliance mon-
itoring because more people will neglect to take
Supplementation is the best short-term interven- regular supplements at prescribed intervals than
tion to improve nutritional health, involving the fortified staple foods. Mineral supplements are
distribution of pills or mineral solutions for imme- prescribed for acute deficiency diseases in
diate consumption. This helps to alleviate acute industrialized countries as well as serving a
mineral shortages but is unsustainable for large niche health market. Zn supplements rank very
populations and should be replaced with fortifica- highly according to the Copenhagen Consensus
tion at the earliest opportunity (Shrimpton and report cost–benefit analysis.

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8 U. Singh et al.

1.3.5 Biofortification greatest long-term cost-effectiveness overall and

is likely to have an important impact over the next
Conventional interventions have a limited few decades. Biofortification is also likely to be
impact, so biofortification has been proposed as more accessible than conventional interventions
an alternative long-term approach for improving in the long term because it removes hurdles such
mineral nutrition (Zhu et al. 2007). Bioforti- as the reliance on infrastructure and compliance.
fication focuses on enhancing the mineral Moreover, plants assimilate minerals into organic
nutritional qualities of crops at source, which forms that are naturally bioavailable and contrib-
encompasses processes that increase both min- ute to the natural taste and texture of the food.
eral levels and their bioavailability in the edible Economic studies have shown many potential
part of staple crops. The former can be achieved health benefits of biofortification strategies, espe-
by agronomic intervention, plant breeding, or cially in combination with conventional strategies
genetic engineering, whereas only plant breeding (Buois 2002; Stein et al. 2008).
and genetic engineering can influence mineral
bioavailability. Plant breeding and genetic engi- 1.3.5.1 Plant Breeding
neering are often compared because, in contrast Plant breeding programs focus on improving the
to agronomic interventions, both involve chang- level and bioavailability of minerals in staple
ing the genotype of a target crop. The two pro- crops using their natural genetic variation
cesses are similar in aim, albeit different in (Welch and Graham 2005). Breeding approaches
scope. Both attempt to create plant lines carrying include the discovery of genetic variation affect-
genes that favor the most efficient accumulation ing heritable mineral traits, checking their stabil-
of bioavailable minerals—plant breeding ity under different conditions, and the feasibility
achieves this by crossing the best performing of breeding for increasing mineral content in
plants and selecting those with favorable traits edible tissues without affecting yields or other
over many generations—whereas genetic engi- quality traits. Breeding for increased mineral
neering accesses genes from any source and levels has several advantages over conventional
introduces them directly into the crop. Plant interventions (e.g., sustainability); no high-
breeding is limited to genes that can be sourced mineral varieties produced by this method have
from sexually compatible plants, whereas genetic been introduced onto the market thus far. This
engineering has no taxonomic constraints and reflects long development times, particularly if
even artificial genes can be used. the mineral trait needs to be introgressed from a
The main advantage of genetic engineering and wild relative. Breeders utilize molecular biology
plant breeding approaches for mineral enhance- techniques such as quantitative trait locus (QTL)
ment is that investment is only required at the maps and marker-assisted selection (MAS) to
research and development stage, and thereafter accelerate the identification of high-mineral
the nutritionally enhanced crops are entirely sus- varieties, but they have to take into account
tainable. Furthermore, as stated above, mineral- differences in soil properties (e.g., pH, organic
rich plants tend to be more vigorous and more composition) that may interfere with mineral
tolerant of biotic stress, which means yields are uptake and accumulation. For example, the min-
likely to improve in line with mineral content eral pool available to plant roots may be
(Frossard et al. 2000; Nestel et al. 2006). Unlike extremely low in dry, alkaline soils with a low
conventional intervention strategies, genetic engi- organic content (Cakmak 2008).
neering and plant breeding are both economically
and environmentally sustainable (Stein 1.3.5.2 Conventional Plant Breeding
et al. 2008). Although there are no commercial This allows crop scientists to make significant
nutritionally enhanced plants derived from either improvement in the nutritional, eating quality,
method at the current time, this approach has the and agronomic traits of major subsistence food

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1 Biofortification: Introduction, Approaches, Limitations, and Challenges 9

crops. Conventional breeding is limited, how- 1.3.5.4 Molecular Breeding

ever, because it can only use the genetic Also called marker-assisted breeding, this is a
variability already available and observable in powerful tool of modern biotechnology that
the crop being improved or occasionally in the encounters little cultural or regulatory resistance
wild varieties that can cross with the crop. Fur- and has been embraced so far even by organic
thermore, conventional breeders usually have to growers because it relies on biological breeding
trade away yield and sometimes grain quality to processes rather than engineered gene insertions
obtain higher levels of nutrition. One example is to change the DNA of plants. This technique is
quality protein maize (QPM), which has taken expanding rapidly with the development of geno-
decades of conventional plant breeding work to mics, which is the study of the location and
develop into varieties acceptable to farmers. function of genes, and with the rapid decline in
However, multiple gains are at times possible, costs of screening plant tissue. Once scientists
as with iron and zinc in rice and wheat, where the have identified the location of a gene for a desir-
characteristics that lead to more iron and zinc in able trait, they build a probe that attaches itself
the plant can also lead, by some accounts, to only to a DNA fragment, a so-called marker,
higher yield. Other biofortified crops, such as unique to that gene. They then can use this
the orange-fleshed sweet potatoes (OFSP) pro- marker as a way to monitor and speed up their
moted through the HarvestPlus program in efforts to move this trait into relatives of the plant
Africa, have been successfully selected and using conventional breeding. For example, since
developed for both nutrient and (at least rainy the marker can be detected in the tissue of new
season) yield traits (Unnevehr et al. 2007). seedlings, the presence or absence of the desired
trait can be determined without having to wait for
a plant to mature, often reducing by years the
1.3.5.3 Mutation Breeding
length of a typical crop development process. If
Mutation breeding has been used extensively in
molecular breeding reduces the number of
developed and developing countries to develop
generations required to develop a pure line vari-
grain varieties with improved grain quality and in
ety by three generations, this can save 3 years of
some cases higher yield and other traits. This
research time. The use of molecular breeding has
technique makes use of the greater genetic
increased dramatically both by private seed
variability that can be created by inducing
companies and government plant breeders in
mutations with chemical treatments or irradia-
developed countries, and it is gradually spread-
tion. The FAO/International Atomic Energy
ing to developing countries (Pray 2006). Using
Agency (IAEA) website contains more than
this technique, plant breeders also can stack into
2500 varieties that have been developed through
one variety several different genes that code for
mutation breeding (Mutant varieties database).
different traits, for example, QPM, disease resis-
Of these, 1568 are in Asia, 695 in Europe, and
tance, and drought tolerance in maize (Pray
165 in the United States. Most of the European
2006). This technique has also been used to find
and US mutants are flowers, but most in Asia are
recessive traits in plants that cannot be located by
basic food crops such as wheat, rice, maize, and
conventional breeding or other techniques.
soybeans. According to their website,
FAO/IAEA include biofortification as one of
the objectives of their mutagenesis program, but 1.3.5.5 Genetic Engineering
there do not seem to be any applicable results yet. Genetic engineering is the latest weapon in the
Varieties produced using mutagenesis can be armory against mineral deficiency and uses
grown and certified as organic crops in the advanced biotechnology techniques to introduce
United States, whereas transgenic crops devel- genes directly into breeding varieties. The genes
oped using recombinant DNA (rDNA) technol- can come from any source (including animals
ogy cannot. and microbes) and are designed to achieve one

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10 U. Singh et al.

or more of the following goals (Zhu et al. 2007): breeding because they make it easier to develop
(a) improve the efficiency with which minerals are crops with multiple desired nutritional traits, main-
mobilized in the soil, (b) reduce the level of tain agronomic viability of biofortified crops,
antinutritional compounds, and (c) increase the adapt agriculture improvements arising in the
level of nutritional enhancer compounds such as United States for obscure crops in developing
inulin. Genetic engineering, or rDNA, is a tech- countries, etc.
nique that offers still greater speed and reach
because it moves specific genes with desired traits 1.3.5.6 Tissue Cultures
from a source organism—one which does not Modern tissue culture techniques can allow
have to be a related organism—directly into the scientists to reproduce plants from a single cell.
living DNA of a target organism. The transgenic These techniques are now used extensively to pro-
trait is added without normal biological reproduc- duce disease-free planting material of clonally
tion, but once in the plant it becomes inheritable propagated crops such as bananas. When tissue
through normal reproduction. Scientists first culture is combined with embryo rescue
developed this technique in the laboratory in techniques, plant breeders can use the genes from
1973 and have been using it to transform agricul- wild and weedy relatives of a crop, which would
tural crop plants since the 1980s. Once a useful normally not cross with the cultivated crop. This
gene has been identified (which can require a allows breeders to increase genetic variability of
major research project and many years), it is the cultivated crop and then bring in valuable traits
attached to both marker and promoter genes and of the wild and weedy relatives. These techniques
then inserted into a plant, usually using a nonvia- have allowed scientists to cross Asian and African
ble virus called Agrobacterium as a carrier. GE rice varieties and develop Nerica rice varieties
produces plants that are known as transgenics or with agronomic traits, such as higher yield and
less precisely as GMOs. GE has great reach resistance to water stresses, that have met with
because it can add valuable characteristics that growing success in Africa. Tissue culture is an
are not currently found in the seeds of individual important tool for propagation of roots and tubers,
plant species. GE was necessary for the develop- such as potatoes and cassava, and both of these
ment of golden rice, which contains the precursor crops are part of current biofortification research.
to VA from a daffodil plant. This was a trait
missing from rice plants, and it could not be
introduced conventionally since daffodils cannot 1.3.6 Microbiological Interventions
be crossed with rice plants. In addition, GE can
take much less time to incorporate desired traits 1.3.6.1 Plant Growth Promoting
into a crop plant than either traditional or molecu- Rhizobacteria (PGPR)
lar breeding. The choice of which technology to These include beneficial bacteria that colonize
use when biofortifying crops comes down to a plant roots and enhance plant growth by a wide
calculation by breeders of how to get the best variety of mechanisms. The use of PGPR is
results most quickly, given their budget constraint. steadily increasing in agriculture, as it offers an
Conventional plant breeding requires less invest- attractive way to reduce the use of chemical
ment in labs or highly trained human resources fertilizers, pesticides, and related agrochemicals
(molecular biologists) than either marker-assisted (Rana et al. 2012). Interventions using PGPR or
selection or genetic engineering, and it faces lower other biological agents are limited. Secretion of
and less costly regulatory hurdles. However, if phytosiderophores by microorganisms and plants
there are no genes for the VA precursors in the in restricted spatial and temporal windows
genome of a crop (as one example), no amount of represents an efficient strategy for uptake of
conventional plant breeding can put them there, iron and other micronutrients by plants from the
and scientists must turn to GE. Molecular breeding rhizosphere. Analysis of the complex
and GE also have advantages over traditional interactions between soils, plants, and microbes

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1 Biofortification: Introduction, Approaches, Limitations, and Challenges 11

in relation with micronutrient dynamics monotropoid, and orchid) are categorized by their
represents a unique opportunity to enhance our distinct morphological characteristics (Wang and
knowledge of the rhizosphere ecology. Such Qiu 2006). Of them, arbuscular mycorrhiza
progress can provide information and tools (AM) is the most common and predominant type.
enabling us to develop strategies to improve Arbuscules, specific “little-tree-shaped” fungal
plant nutrition and health with decrease in the structures inside root cortical cells, serve as the
application of chemical inputs. Microorganisms main sites of nutrient exchange between the plant
are known to differ significantly in competing and the fungus. AM also has external hyphae that
with higher plants for micronutrients (Steven provide an extensive surface area or network for
1991). Among bacteria, a lot of attention has nutrient uptake from soils. Thus, AM is the most
been dedicated to the siderophore-mediated iron important mycorrhiza in agriculture and closely
uptake by fluorescent pseudomonads. A number relates to human nutrition. Obligately depending
of other mechanisms are also involved in the on plant photosynthates as energy sources, the
sequestration and transformation by extensive AM mycelial systems (the vegetative
microorganisms in soil such as production of parts of the fungus) effectively explore soil
acids, alkalis, etc. PGPR constitute a significant substrates and acquire soil inorganic nutrients,
part of the protective flora that benefit plants by including major macronutrients N, P, and K and
enhancing root function, suppressing disease, micronutrients Cu, Fe, and Zn (Caris et al. 1998),
and accelerating growth and development with some capacity for acquiring organic N and P
(Glick 1995). Microorganisms differ in compet- (Koide and Kabir 2000). These soil-derived
ing with higher plants for micronutrients. Species nutrients are not only essential for AM develop-
of Azotobacter differed in their competitiveness ment but are also partly transferred to the host
with wheat plants in extracting Fe and Zn plant. It is believed that many plants that usually
(Shivay et al. 2010). Biofortification of crops form this symbiotic relationship would be unable to
through application of PGPR can be therefore survive without the mycorrhiza. Mycorrhizal
considered as a possible supplementary measure, mycelia and their exudates also constitute a large
which along with breeding varieties can lead to carbon source (20–30 % total soil microbial bio-
increased micronutrient concentrations in wheat mass) for the functioning of other belowground
crop, besides improving yield and soil fertility. microorganisms that ameliorate soil nutrient avail-
ability through decomposition of organic
1.3.6.2 AM Fungi compounds and weathering of inorganic materials.
Most plants, including all major grain crops and So, not only do the activities of AM fungi have
almost all vegetables and fruits, are associated with multiple functions that enhance plant performance
mycorrhizal fungi that improve the uptake of essen- but they also play crucial roles in the development
tial mineral elements from soils and, therefore, of soil properties and the health of the entire
enhance plant growth and productivity. These sym- ecosystem.
biotic fungi, therefore, change, directly or indi-
rectly, the mineral nutrition of plant products that
are also essential for humans. However, the role of 1.3.7 Agronomic Intervention
mycorrhizas on element biofortification may be
piloted through agricultural practices. Mycorrhizas Farmers have applied mineral fertilizers to soil
can potentially offer a more effective and sustain- for hundreds of years in order to improve the
able element biofortification to curb global human health of their plants, but within certain limits
malnutrition. Approximately 90 % of land plants the same strategy can also be used to increase
form mycorrhizas (literally “fungus roots”): they mineral accumulation within cereal grains for
exist everywhere, from tiny home gardens to large nutritional purposes (Rengel et al. 1999). This
ecosystems (Smith and Read 1997). Six types of strategy only works if the mineral deficiency in
mycorrhizas (arbuscular, arbutoid, ecto-, ericoid, the grain reflects the absence of that mineral in

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12 U. Singh et al.

the soil and if the mineral fertilizer contains symptoms, soil and plant tissue tests, and crop
minerals that are rapidly and easily mobilizable. growth responses are principal nutrient disorder
Also, even if plants can absorb minerals effi- diagnostic techniques. Soil applications of
ciently from the soil, they may store the mineral fertilizers are mainly done on the basis of soil
in leaves but not fruits or seeds, or they may tests, whereas foliar nutrient applications are
accumulate the mineral in a form that is not mainly done on the basis of visual foliar
bioavailable, thus having no impact on nutrition symptoms or plant tissue tests. Hence, correct
(Frossard et al. 2000). Like supplements and diagnosis of nutrient deficiency is fundamental
fortification, agronomic intervention is probably for successful foliar fertilization. In addition,
best applied in niche situations or in combination there are some more requirements for successful
with other strategies (Cakmak 2008). One draw- foliar fertilization. Foliar fertilization requires
back of agronomic intervention is the cost and higher leaf area index for absorbing applied
impact of the fertilizers. Fertilizer use is likely to nutrient solution in sufficient amount; it may be
increase the cost of food, thus reducing its avail- necessary to have more than one application
ability to the most impoverished people. The depending on severity of nutrient deficiency.
expensive fertilizers must be applied regularly,
with no direct yield incentive to farmers in devel- 1.3.7.1 Parboiled Rice
oping countries, so the intervention would likely Fe fortification in parboiled rice is a rapid and
be omitted to save costs even though seeds pro- cost-effective solution to Fe deficiency anemia in
duced under rich mineral conditions germinate economically disadvantaged populations with
more vigorously than those in poor soils rice as the major staple food and poor access to
(Cakmak 2008). There is also concern about the animal proteins. It focused initially on the feasi-
impact of increased fertilizer use on the environ- bility of this innovative approach, by examining
ment (Graham 2003). the effectiveness of Fe fortification and retention,
Agronomic strategies to increase the the solubility of Fe in the grain in response to
concentrations of mineral elements in edible fortification treatments, and the likely pathway of
tissues generally rely on the application of min- Fe movement into the endosperm. NaFeEDTA
eral fertilizers and/or improvement of the solubi- has been recently approved as an ingredient to be
lization and mobilization of mineral elements in used in supervised food fortification programs
the soil (White and Broadley 2009). When crops (Hurrell 2003) and is the most promising Fe
are grown where mineral elements become fortification compound for food additives and is
immediately unavailable in the soil, targeted used intensively to prevent oxidation and color
application of soluble inorganic fertilizers to changes in food and promote its bioavailability in
roots or to leaves is practiced. In situations the human diet. The effectiveness of enhancing
where mineral elements are not readily Fe density in white rice through the Fe-fortified
translocated to edible tissues, foliar applications parboiling process is far greater than that
of soluble inorganic fertilizers are made. It has achieved from conventional and transgenic rice
been observed that the human population of the breeding. For example, Fe concentration in
world has exceeded the carrying capacity of milled rice of IR68144-2B-2-2-3, an improved
low-input agriculture, and modern inorganic rice cultivar by conventional breeding, is
fertilizers are necessary to obtain the crop yields 7–13 mg Fe kg−1 (Graham et al. 1999) and
required to prevent starvation (Graham 37 mg Fe kg−1 in rice containing transferred
et al. 2007). Essential plant nutrients are mainly soybean ferritin gene (Vasconcelos et al. 2003).
applied to soil and plant foliage for achieving In contrast, Fe concentration in the milled rice
maximum economic yields. Soil application grains Fe fortified in the parboiling had 70–144
method is more common and most effective for and 30–110 mg Fe kg−1 in 60 and 120 s milled
nutrients, which are required in higher amounts. grains, respectively.
However, under certain circumstances, foliar fer- Comparatively, a substantial loss of Fe
tilization is more economic and effective. Foliar sprayed on raw rice surface occurs if the rice is

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1 Biofortification: Introduction, Approaches, Limitations, and Challenges 13

rinsed before cooking. Although a polymer coat- These efforts are now being complemented with
ing technique has been advocated for painting Fe the introduction of molecular markers (QTL
on the rice grain surface to minimize Fe loss from mapping and MAS) as tools to increase breeding
washing and/or cooking, these techniques are efficiency (Hash et al. 2003). Progress has also
expensive and not practical in rice mills of devel- been reported for a completely different approach
oping countries. In comparison, parboiled rice is to improving cereal nutrient availability. In trans-
a rapid and cost-effective vehicle to deliver Fe genic animals like the Enviropig, phytase is pro-
nutrition benefits through the already established duced in the salivary glands and the active enzyme
parboiling infrastructure, market network, and is secreted into the saliva (Forsberg et al. 2003).
consumers’ acceptance in Asia (particularly in These pigs show improved phosphorus uptake.
the subcontinent) and Africa, where the high Such a transgenic pig might also show improved
risk of Fe malnutrition-induced anemia is present iron uptake in the intestine, owing to lower content
(Graham et al. 1999). Most of the fortified Fe in of the antinutritional phytate.
the milled rice grains remained in the dilute acid-
soluble pool, which is considered as potentially
bioavailable in the human diet in all cultivars. 1.4 Hindrances or Limiting Factors
One of the significant advantages of parboiled
rice is that parboiling resulted in a significant 1.4.1 Antinutrients
inward movement of the fortified Fe into the
endosperm, countering milling-induced Fe loss Phytate and tannins are the limiting factors in the
in raw rice grains due to restricted distribution of absorption of Fe, Zn, and Ca by the gut (Mendoza
Fe in the aleurone and embryo (the bran fraction) 2002). Phytate occurs widely in plant tissues but is
of brown rice (Bhattacharya 2004). Parboiling concentrated in seeds or grain. There is consider-
itself may cause inward migration of some min- able intraspecific variation in phytate concentra-
eral nutrients present in the surface layers of rice tion in edible portions (Glahn et al. 2002; Coelho
grain, resulting in a higher retention rate of these et al. 2005) that is independent of variation in Fe
nutrients when being milled to produce white and Zn concentrations. In addition, several low
rice (Ali and Bhattacharya 1980; Palipane and phytic acid (lpa) mutants have been produced by
Swarnasiri 1985), such as P, Ca, Fe, Mn, Mo, and non-transgenic techniques in rice, maize, wheat,
Cr in milled parboiled rice. barley, and soybean (Banziger and Long 2000).
Fortuitously, plants with lpa mutations often show
raised levels of seed Fe, Zn, and Mg (or similar
1.3.8 Biofortification of Feed levels to those found in wild type), although they
for Livestock do have reduced concentrations of seed
Ca. Tannin concentration in edible tissues also
For many decades plant breeding primarily varies greatly between varieties (Lin et al. 2005).
focused on yield, and little attention was given to Hence, breeding for reduced concentrations of
the nutritional value of cereal residues (bran and these antinutrients appears feasible.
straw) that were not used for human consumption. Phytic acid, as well as other metabolites pro-
However, bran and straw are among the most duced by plants, such as PP, is considered an
important feed for ruminant livestock in many “antinutrient” because by chelating iron, it can
parts of the world, where sorghum and millet are reduce its absorption in the human gut (Jin
important staple cereals in addition to rice and et al. 2009). In plants, however, phytic acid
wheat. In sorghum and pearl millet, various crop fulfills essential biological functions (Murgia
management interventions (Reddy et al. 2003) and et al. 2012). Phytate, a mixed cation salt of
plant breeding (Zerbini and Thomas 2003) D-myo-inositol, hexakisphosphate, commonly
strategies were shown to influence yield and known as PA, InsP6, or IP6, constitutes up to
improve quality of the straw for animal feed. 1–8 % of mature seed dry weight and accounts

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14 U. Singh et al.

for up to 90 % of phosphorus content in cereal Table 1.1 Mineral nutritional enhancers and
grains, legumes, nuts, and oil seeds. Phytate antinutrients
represents an important metal cation reserve Nutritional enhancers Antinutrients
(magnesium, potassium, calcium, manganese, b-Carotene (provitamin A) Oxalic acid
barium, and iron) in seeds, either in the aleurone (oxalate)
Inulin Phytic acid
cell layer or in the seed embryo, depending on the
(phytate)
plant species. Degradation of phytate occurs dur- Long-chain fatty acids Polyphenols
ing seed germination, by means of phytases, a Certain amino acids (cysteine, Tannins
class of phosphatases capable of releasing at lysine, etc.)
least one phosphate from phytic acid (IP6) Certain organic acids (ascorbic acid, Others
(Bohn et al. 2008). The consequent release of citrate, etc.)
phosphorus and mineral nutrients supports growth Vitamin D Others
and development of the seedling. Besides its well- Adapted from White and Broadley (2005); Welch and
Graham (2005)
known role in mineral storage in seeds, IP6 also
acts in the leaves in the signaling cascade trig-
gered by drought/osmotic stress leading to stoma- concentration in cassava varied by 250-fold in
tal closure. In guard cells ABA produces rapid leaves and 40-fold in roots among the
changes in IP6 which trigger release of Ca2+ 530 accessions of the CIAT core collection,
from endomembrane stores and inhibition of K+ whereas b-carotene concentration varied by 3.7-
inward rectifying channels. Some low IP6 cereals fold in leaves and 10-fold in roots. Similarly, ascor-
are less tolerant to stress and possess undesirable bate concentration varied almost 20-fold among
agronomical traits, such as reduced seed yield and Dioscorea alata accessions. There is also apprecia-
lower seed viability, as observed in bread wheat ble intraspecific variation in amino acid
(Triticum aestivum), rice (Oryza sativa), and bar- concentrations in edible tissues (Guzman-
ley (Hordeum vulgare) (Zhao et al. 2008), Maldonado et al. 2000). However, the complement
suggesting that IP6 is indeed involved in essential of amino acids present in different foodstuffs is
biological functions in the whole plant. More constrained by evolutionary heritage such that
recently, a key role for IP6 in the maintenance of cereal and vegetable crops contribute complimen-
basal resistance against a wide range of pathogens tary amino acids to the diet (White and Broadley
has been demonstrated transgenic potatoes with 2005).
compromised synthesis of IP6 (through IPS anti-
sense RNA) are less resistant to virus infection.
Disruption of IP6 biosynthesis in Arabidopsis is
also associated with increased susceptibility to 1.5 Assessing Iron Bioavailability
viruses and to bacterial and fungal pathogens from Biofortified Foods
(Murphy et al. 2008).
Iron bioavailability from biofortified food can be
assessed through four different approaches:
1.4.2 Promoters (i) algorithmic approximations, (ii) in vitro diges-
tion and Caco-2 intestinal cell uptake assay, (iii)
Some organic compounds stimulate absorption of animal studies, or (iv) human studies (Cockell
essential mineral elements by humans (Table 1.1). 2007; Fairweather-Tait 2001). The algorithmic
These include ascorbate (vitamin C), b-carotene method is the least suited to predict the effects of
(provitamin A), protein cysteine, and various new circumstances, such as the nutritional impact
organic and amino acids. There is considerable of a new biofortified crop. By contrast, the choice
intraspecific variation in both ascorbate and between the remaining methods should take into
b-carotene concentrations in fruit and vegetables account experimental costs, short- and long-term
(Frossard et al. 2000). For example, ascorbate responses, and differences in iron absorption

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1 Biofortification: Introduction, Approaches, Limitations, and Challenges 15

between laboratory animals and humans (Cockell seeds rich in trace elements are stronger to resist
2007; Walter et al. 2003). It is however important against biotic and abiotic stresses including
to note that at least two types of human bioassays diseases and environmental stresses (Bouis
for bioavailability have qualified as necessary: 2003). Further, fortified or enriched seeds also
efficacy and effectiveness trials. Efficacy trials have more plant vigour, seedling survival, faster
assess the beneficial effect of iron biofortification initial emergence and grain yield.
under ideal conditions and thus depend only on
biological factors (such as in clinical trials); effec-
tiveness trials take into account behavioral factors, 1.7 Future Challenges
because trials are performed under “real-life
situations” (Davidsson and Nestel 2004). • Produce crops for human nutrition with
increased iron concentration. Biofortification
strategies alternative to reduction in concen-
1.6 Biofortification: Strategic
tration of phytic acid or polyphenols should be
Advantages
explored further, in order to increase iron
absorption without loss of their beneficial
The biofortification strategy seeks to take advan-
effects. When overexpressing ferritin, such
tage of the consistent daily consumption of large
crops should be tested for concentration of
amounts of food staples by all family members,
various heavy metals, in laboratory as in
including women and children who are most at
open-field trials, before releasing to the pub-
risk for micronutrient malnutrition. As a conse-
lic. Detailed knowledge on mechanisms
quence of the predominance of food staples in
regulating iron compartmentalization in vari-
the diets of the poor, this strategy implicitly
ous plant organs will offer a major contribu-
targets low-income households.
tion for reaching such goal.
After the one-time investment is made to
develop seeds that fortify themselves, recurrent • Expand research on prebiotics and iron absorp-
costs are low and germplasm may be shared tion. Crops biofortified with prebiotics have the
internationally. It is this multiplier aspect of potential to partially circumvent the “iron par-
plant breeding across time and distance that adox” caused by host–pathogen competition
makes it so cost-effective. Once in place, the for iron, by favoring amelioration of gut health
biofortified crop system is highly sustainable. and gut-associated immune defense.
Nutritionally improved varieties will continue • Promote initiatives supporting large-scale
to be grown and consumed year after year, even prospective studies on the effects of iron
if government attention and international funding biofortified crops on effectiveness of the
for micronutrient issues fade. Moreover, bioforti- adopted biofortification strategy in relieving
fication provides a truly feasible means of iron deficiency anemia and in improving gen-
reaching malnourished populations in relatively eral health.
remote rural areas, delivering naturally fortified • Improve the efficiency with which minerals
foods to people with limited access to commer- are mobilized in the soil.
cially marketed fortified foods, which are more • Improve the efficiency with which minerals are
readily available in urban areas. taken up from the soil into the roots of the plant.
Biofortification and commercial fortification, • Improve the transport of minerals from the
therefore, are highly complementary. Breeding roots to storage tissues, such as grain.
for higher trace mineral density in seeds will • Increase the capacity of storage tissues to
not incur a yield penalty. In fact, biofortification accumulate minerals in a form that does not
may have important spin-off effects for increas- impair plant vegetative growth and develop-
ing farm productivity in developing countries in ment, but remains bioavailable for humans.
an environmentally beneficial way. Mineral- • Reduce the level of antinutritional compounds
packed seeds sell themselves to farmers because, such as phytic acid, which inhibit the absorp-
as recent research developments proved that tion of minerals in the gut.

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16 U. Singh et al.

Glossary hunger, they usually refer to those who, for

sustained periods, are unable to eat sufficient
Anemia condition in which the number of red food to meet basic nutritional needs
blood cells or their oxygen-carrying capacity Food fortification with iron a way to increase
is insufficient to meet physiological needs. iron concentration in food by adding an iron
The number of red blood cells is dependent compound (e.g., ferrous sulfate heptahydrate,
on age, gender, and altitude and is altered by ferrous gluconate, and sodium FeEDTA
smoking, or during pregnancy the hemoglobin among others) to processed food (e.g., infant
threshold used to define anemia is <11 g/dL formula or cereals, wheat flour products, and
Antinutrient a substance that impairs the corn meal among others)
absorption of an essential element by the gut Fortification the addition of an ingredient to
Bioavailability measure of fractional utilization food to increase the concentration of a partic-
of orally ingested nutrient and also defined as ular element
the proportion of a particular nutrient that can Malnutrition the condition that results from
be used by the body to provide its associated eating a diet in which certain nutrients are
biological function. In simple words it is the lacking, in excess (too high in intake), or in
amount of an element in a food constituent or the wrong proportions. The verb form is
a meal that can be absorbed and used by a “malnourish”; “malnourishment” is some-
person eating the meal. Bioavailability also times used instead of “malnutrition.” A num-
refers to the portion of an ingested nutrient ber of different nutrition disorders may arise,
that can be absorbed in the human gut. The depending on which nutrients are under- or
bioavailability of minerals can be reduced or overabundant in the diet. In most of the
enhanced by the consumption of food rich in world, malnutrition is present in the form of
antinutrients (inhibitors of absorption) or undernutrition, which is caused by a diet
nutritional enhancers, respectively lacking adequate calories and protein and not
Biofortification process for improving the enough food, and of poor quality. Extreme
nutritional value of the edible parts of the undernourishment is starvation, and its
plants, through mineral fertilization, conven- symptoms and effects are inanition. While
tional breeding, or transgenic approaches. It malnutrition is more common in less devel-
can also be defined as the process of increas- oped countries, it is also present in
ing the bioavailable concentrations of an ele- industrialized countries. In wealthier nations
ment in edible portions of crop plants through it is more likely to be caused by unhealthy
agronomic intervention or genetic approaches diets with excess energy, fats, and refined
Disability-adjusted life year (DALY) a time- carbohydrates (WHO 2001)
based parameter for assessing global burden Promoter a substance that stimulates the
of disease that combines years of life lost due absorption of an essential element by the gut
to premature mortality (years of life lost, YLL) Reference nutrient intake (RNI) the amount of
and years of life lost due to time lived in states an element that is enough, or more than
of less than full health (years lived with dis- enough, for most people in a group (usually
ability, YLD): DALY¼YLL+YLD at least 97 %). If the average intake of a group
Hidden hunger the term “hidden hunger” has is at the RNI level, then the risk of deficiency
been used to describe the micronutrient mal- in the group is small
nutrition inherent in human diets that are ade- Regulators organic compounds, either natural
quate in calories but lack vitamins and/or or synthetic, are able to modify or control
mineral elements plant growth and/or development. Also, plant
Hunger the physical sensation of desiring food. growth regulators (PGRs)
When politicians, relief workers, and social Supplementation the addition of an element to
scientists talk about people suffering from the diet to make up for an insufficiency

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1 Biofortification: Introduction, Approaches, Limitations, and Challenges 17

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