Carotenoids in staple foods: Their potential to improve
human nutrition
Robin D. Graham and Julia M. Rosser
Abstract
As part of the Consultative Group on International
Agricultural Research (CGIAR) Micronutrients Project,
we have investigated the content of carotenoids in staple
foods, particularly wheat. Wheat varies widely in carote-
noid content, depending on the variety and type. Durum
(pasta) wheat is generally higher in carotenoid content,
because the market has continued to demand strong
pigment in pasta and noodle products, whereas in bread
wheat the market demands flour as white as possible.
Consequently, twentieth-century wheat breeders have
consciously selected wheat varieties low in carotenoid
content, although older, high-carotenoid bread wheats
are still available and the trait is not lost. The entire
carotenoid biosynthetic pathway exists in wheat grains,
so varieties high in β-carotene and/or other carotenoids
can be reintroduced if and when education in nutrition
creates the demand. Numerous high-yielding maize
varieties high in β-carotene already exist and have been
used to eliminate vitamin A deficiency in livestock. A
β-carotene–rich rice has been genetically engineered
recently. Although the carotenoid content of beans has not
yet been explored, high– β-carotene lines of cassava exist,
and the trait is easily handled in a breeding programme.
Yellow types of most staples are known, for example,
sorghum, potatoes, and sweet potatoes. The amounts
present are such that we can assert that vitamin A
deficiency could easily be eliminated globally by deliver-
ing the required amounts via food staples. Moreover,
there are strong signs that other benefits in eye health,
enhanced absorption of iron from non-haem sources,
anticarcinogenic effects, enhanced aroma, and better
storage life may also result.
Introduction
The world is awash with carotenoid pigments manu-
The authors are affiliated with the Department of Plant
Science, University of Adelaide, in Glen Osmond, South
Australia.
404 Food and Nutrition Bulletin, vol. 21, no. 4 © 2000, The United Nations University.
factured by all green plants in order to, among other
things, protect chlorophyll from photodestruction
by solar radiation at wavelengths it cannot utilize.
The carotenoids absorb this green light and fluoresce
it again at longer wavelengths so that it can then
be absorbed by chlorophyll and converted to usable
energy, namely, sugar. So fundamental is this photo-
protective role that many herbicides act by inhibiting
carotenoid synthesis [1]. Many non-photosynthetic
tissues, notably storage tissues that constitute our
staple foods, also contain carotenoids. In storage
roots it is obvious that the pigments are not needed
for harvesting light but may well perform a role as
antioxidants, contributing to storage life.
There are two major classes of carotenoid pigments
in plants: the carotenes, which are hydrocarbon chains
with no hydroxyl side chain, and the xanthophylls,
which are similar in structure but have hydroxyl side
chains on their terminal rings. Figure 1 shows the
structure of lycopene, α- and β-carotene, zeaxanthin
and lutein, and retinol (vitamin A). The relation
of retinol to βcarotene is obvious: cleavage of the
β-carotene molecule exactly in the middle at the double
bond yields two 20-carbon molecules of retinol.
Because α-carotene is not symmetrical like
β-carotene, only one molecule of retinol is produced
when it is cleaved in the middle, so α-carotene is only
half as efficient as β-carotene in producing vitamin A
in the human body. Because these carotenes are highly
reactive antioxidants, not all of the ingested carotene
will survive to be cleaved to produce vitamin A. It is
generally considered that the human body can gener-
ate one molecule of retinol from each six molecules
of β-carotene metabolized, and that conversion of
α-carotene to retinol is about half as efficient as that of
β-carotene. Lower conversion rates have been reported.
There are four other carotenes that can be converted to
retinol, but at even lower efficiencies than α-carotene
and β-carotene.
The biosynthetic relationships among the caroten-
oids are shown in figure 2. Lycopene is the red pigment
of tomatoes, and two separate pathways continue on
Carotenoids in staple foods
CH2OH
β-ring Retinol
β-carotene
α-carotene
Lycopene
OH
Zeaxanthin
HO OH
Lutein
HO
FIG. 1. Structures of important carotenoid pigments in
plants and of retinol, showing that a β-ring is characteristic
of both retinol and α- and β-carotene. Retinol is produced
from α-carotene and β-carotene in the mammalian liver and
intestinal mucosa
from it, leading to most of the important carotenes
and xanthophylls in plant chloroplasts.
Millions of people in developing countries who rely
heavily on grain products to meet their energy and
protein requirements suffer from vitamin A deficiency,
resulting in blindness, poor immune function, and
early death [2]. In the lowest socio-economic strata
of society, the relatively low cost of staples as a source
of energy means that they constitute most of the
diet. With some exceptions, this would appear to be
because the major staples—wheat, rice, maize, cassava,
potatoes, and sorghum—are white, starchy foods with
few provitamin A carotenoids present. It appears that
this may not always have been the case. Yellow types of
all these staples are known, at least in the germplasm
banks of the world, and appear to be more the norm
for staples before the rise of modern plant-breeding
efforts in the twentieth century. In some cases, yellow
Vitamin
A α-carotene
Zinc Iron
FIG. 3. Potential interactions in the absorption and metabo-
lism of iron, zinc, and vitamin A in humans
405
types are still common. Yellow cassava is known in
northern Brazil and preferred as a fresh vegetable to the
white types that are used for flour. Yellow maize, con-
taining large amounts of β-carotene, is quite common
and was bred in the United States some 40 years ago to
cure hogs of vitamin A deficiency. However, like other
staples, it is often not the choice for human consump-
tion, perhaps because it is identified with animal feed,
or because white flour is seen to be uncontaminated
by soil, faecal material, or cheaper diluents.
Recent reports [3–5], suggesting that a relatively
small supplement of vitamin A or β-carotene can
double the absorption of endogenous non-haem iron
from cereal meals, greatly increase the significance of
carotenoids in staples. Carotenoids may be important
not only in controlling vitamin A deficiency itself,
but also in controlling the more ubiquitous and insidi-
ous iron-deficiency anaemia. Thus, a survey of the
carotenoid content of current cultivars and germplasm
bank resources of the major staples is needed to assess
the potential to deliver health-related carotenoids to
resource-poor populations who are isolated either
geographically or socio-economically and heavily
dependent on staples for food. This paper addresses
the situation in the cereals, with emphasis on wheat.
Nutrient interactions involving iron, zinc,
and vitamin A
The potential for synergistic interactions among three
nutrients is shown in figure 3. Each corner of the
triangle represents the main effect of one nutrient
of this particular group of three nutrients that are
of interest because they are among the most widely
Lycopene
δ-carotene γ-carotene
β-carotene
α-cryptoxanthin β-cryptoxanthin
Lutein Zeaxanthin
FIG. 2. Both α- and β-carotene are derived from lycopene
via separate biosynthetic pathways. Through hydroxylation,
the carotenes are converted to the oxygenated group of
carotenoids known as xanthophylls
406
deficient in human populations [2, 6–8] and their
density can be increased in staples by plant-breeding.
Each side of the triangle represents the first-order
interaction of a pair of nutrients, and there is the
potential for a second-order interaction among all
three nutrients. An interaction is recognized when
the response of an individual to one nutrient is not
constant but varies depending on the level of another
nutrient. In terms of nutrition and health, the essential
roles (main effects) of these three nutrients are well
known and do not need to be repeated here.
Zinc–vitamin A interactions
Evidence of interactions between vitamin A and zinc
emerged in the late twentieth century (see reviews by
Christian and West [9], and Solomons and Russell
[10]). In their summary figure, Christian and West
[9] indicated a role of zinc in synthesis of retinol-
binding protein (RBP), increasing lymphatic absorp-
tion of retinol and its inter- and intracellular transport,
whereas vitamin A affects the synthesis of a zinc-
dependent binding protein and thus the absorption
and lymphatic transport of zinc. The interaction of
delivering these two essential nutrients together to
patients deficient in both was shown by Udomkesmalee
et al. [11], in that they observed strong synergistic
effects of adding both nutrients together on eye param-
eters and RBP. They concluded that the dual treat-
ment was so effective that supplementation with only
one dose containing twice the recommended daily
allowance of each was sufficient to normalize the
cohort. We argue that plant-breeding can also double
the normal daily dose of these nutrients delivered by
today’s staples.
Iron–zinc interactions
Interactions of the mineral–mineral type among
chemically relatively similar members of the transition
metal series in both plants and animals have been
characterized much earlier than the zinc–vitamin A
type just mentioned (see Hill and Matrone [12]). Both
synergistic and antagonistic interactions occur, but
the competition of Fe2+ with Zn2+ for the bond with
plasma transferrin is an antagonistic interaction that
is well documented [13]; however, this effect is less
likely to be significant if the subject is deficient in these
nutrients. Recently, evidence of synergy in absorption
generated by genetically different beans was identified
(see King et al. [14] in these proceedings). The amount
of iron absorbed by young women from two different
beans of similar iron density was greater for the beans
with the higher zinc density, and this could not be
explained alternatively by the levels of phytate or
tannins. Such a synergistic effect strongly indicates
breeding for staples dense in both iron and zinc in
R. D. Graham and J. M. Rosser
order to address iron-deficiency anaemia effectively.
Vitamin A–iron interactions
Interest in this interaction has been kindled by the
recent article by Garcia-Casal et al. [3], who showed
that just 500 IU of vitamin A or β-carotene added to a
0.1-kg meal of cereal (wheat, rice, or maize) doubled
the iron absorption from the gut of human subjects in
Venezuela. Earlier work [5, 15, 16] suggests that this
effect occurs in the presence of non-haem, phytate-
bound iron and may be due to reduction and/or chela-
tion of iron by the carotenoid, enhancing transport
of iron from the lumen of the gut to the mucosal cell
membrane. It appears that in the presence of high
levels of phytate and tannins in the diet, vitamin A
or β-carotene will enhance the bioavailability of iron
in humans, but in the absence of these antinutrients,
no enhancement was found [Welch RM, House WA,
Glahn R, Garvin D, personal communication, 11 Sep-
tember 1999]. A further question arises as to whether
the xanthophylls that are not precursors to vitamin A
might also function to give this synergistic response,
and perhaps function even better than β-carotene, if
complex formation is the mechanism, as suggested by
Garcia-Casal et al. [3].
A putative second-order interaction
Although the study may be technically difficult, a
three-way interaction, in which the response to one
nutrient depends on the levels of the other two nutri-
ents, can be predicted. Given the synergies in all three
first-order interactions, a person with a deficiency
of all three nutrients can be expected to respond dra-
matically to relatively small supplements of the three
nutrients given together until normal homeostasis
is reached. This is because the absorption efficiency
is likely to be very high for each, and with more of
each available to catalyse the primary functions of
the other, symptoms will be quickly suppressed. Put
differently, the body has less tolerance to a deficiency
when it occurs together with a deficiency of one or
more synergistic nutrients. This principle is consistent
with the finding of Udomkesmalee et al. [11], surpris-
ing to them, that only a relatively small supplement
of both nutrients, zinc and vitamin A, was needed to
normalize the diagnostic indices.
Genetics
Little definitive information on the genetics of inherit-
ance of carotenoid content is available, except for car-
rots, in which three major genes controlling primary
colour classes and other conditioning loci have been
Carotenoids in staple foods
described [17]. Three basic biosynthetic enzymes are
involved [18]. Seven major biosynthetic steps, and
more than 20 genes, have been well characterized in
the synthesis of carotenoids in tomatoes [19]. Hauge
and Trost [20] described a major gene for carotene
content in maize that is incompletely dominant and
designated it the Y (yellow) locus.
Carotenoids of wheats
In order to breed wheat varieties with an enhanced
carotene content, we need to understand the develop-
ment of carotenoids in the wheat grain and the genetic
variation in the biosynthetic process that could be
exploited. The use of bread wheat as a staple in many
regions where vitamin A deficiency is prevalent indi-
cates that there is a need for identification and quanti-
fication of the carotenes present in wheat germplasm.
The most accurate method of identification of
the many carotenoids that are present in biological
material is high-performance liquid chromatography
(HPLC). This accuracy is needed because each carotene
has a different provitamin A activity, indicating its
usefulness in the treatment of deficiencies. HPLC is
especially valuable in the analysis of carotenes that are
light, heat, and oxygen sensitive. A method of extract-
ing carotenoids from wheat grain flour was established
by comparing a number of solvents and extraction
procedures to find the most efficient method that was
also compatible with HPLC analysis. HPLC was used to
distinguish between xanthophylls and the provitamin
A carotenes. All procedures were conducted under
nitrogen gas to prevent oxidation of carotenes.
11
10
9
Carotenoids (mg/kg)
8 Lutein
7 β-carotene
6 α-carotene
5 200
4
3
2 0
1
0
0 10 20 30 40
Days after anthesis
FIG. 4. Time trend of synthesis and metabolism of various
carotenoids in the caryopsis of wheat (var. Krichauff) from
anthesis to maturity
407
The appearance of carotenoids in the wheat grain
during development and maturation was studied by
the sequential harvest of grains from anthesis to full
grain hardness. Figure 4 shows that total carotenoids
reach a maximum 12 to 15 days after anthesis, and
thereafter the concentrations decline. Both α-carotene
and β-carotene decline to low levels at maturity, while
lutein remained at measurable levels. This proves
that the whole biosynthetic pathway exists in the
endosperm of wheat and that recombination of genetic
loci involved in the expression of each of the enzymes
should be able to enhance the levels shown by 10
to 100 times. If the hydroxylation enzymes were sup-
pressed, more carotenoid would be left as provitamin
A, and the daily requirement should be deliverable in
the normal daily intake of wheat products.
Bread and durum (pasta) wheats were analysed
by HPLC; the range of concentrations found is rep-
resented in figure 5. These amounts are perhaps 20
times less than in a range of vegetables and fruits,* but
the greater consumption of staples would make them
more equal suppliers of carotenoids in the diet.
The carotenoid-dense lines of durum wheats, if
all carotenoid were present as β-carotene, would be
enough to supply the daily requirement (1–2 mg/kg
of wheat products.
Carotenoids of rice
Ye et al. [21] have produced yellow endosperm trans-
genic rice grain containing β-carotene. Four genes
* Rosser JM, Khachik F, Graham RDG. Paper presented
at the 12th International Carotenoid Symposium, Cairns,
Australia, 18–23 July 1999.I moved this from the refs. (no.
21). Is there a published version?
400
300
Lutein
Total VA carotenoids
g/kg
100
BW1 BW2 BW3 BW4 BW5 DR1 DR2 DR3
Wheat variety
50 FIG. 5. Carotenoid concentrations of five bread wheats (BW)
and three durum wheats (DR), representing the range of
values found in collections from the germplasm banks in
the Centro Internacional de Mejoramiento de Maiz y Trigo
(CIMMYT) and the International Center for Agricultural
Research in the Dry Areas (ICARDA)
408
in two constructs, two from daffodil and two from
the bacterium Erwina uredovora, were added to the
rice line to complete the biosynthetic pathway to
β-carotene. The resulting transgenic rice line synthe-
sized enough β-carotene in the endosperm to meet
part of the vitamin A requirements of people depend-
ent on rice as a staple in South Asia. The insertion
of these genes into rice to express β-carotene was
necessary because parts of the pathway had been lost,
while their own evidence suggests that downstream
parts of the pathway were still expressed.
Recently, “yellow” rice that may supply the missing
genes naturally was discovered in the International
Rice Research Institute (IRRI) germplasm bank. On
the advice of Prof. Lita del Mundo of the University
of the Philippines, Los Baños, a search was made for
amarillo (Spanish for yellow), and two entries were
found, one from the Philippines and one from Cuba.
The HPLC analyses of the pigments is under way.
The endosperm is vitreous; one line appears to have
pigment through half and the other through 90% of
the endosperm, the rest being white “belly” or starchy
endosperm. If so, further enhancement of expression
should be possible by recombination between the two
lines, and incorporation into the new high-iron, high-
zinc, high-yielding variety should not take more than
a few years.
Carotenoids of maize
White maize is frequently preferred for human con-
sumption, and yellow types are preferred for animal
feed. The stigma associated with this appears to be one
barrier to the adoption of yellow maize for human
consumption. Other colours are acceptable for human
consumption, notably the highly prized blue maize
in Mexico.
In maize, the total carotenoids varied by a factor
of 2.5 between the means of six high-carotene and
six low-carotene inbred lines, and their provitamin
A activity varied by a factor of 4.4; even wider vari-
ation was found between means of single crosses
made within these groups (table 1). Yellow corns have
been recognized for decades as the main source of
provitamin A for hogs and other farm animals relying
on winter feed rations, and some effort has been put
R. D. Graham and J. M. Rosser
into breeding for this trait already [22]. Where yellow
maize is already accepted in the marketplace, further
enhancement of its provitamin A content could have
an immediate positive impact on dietary intakes [23].
Conclusions
Carotenoids are abundant in the plant kingdom, not
only in green tissues but in storage tissues as well,
including most of the major staples. Both the provi-
tamin A carotenes and the non-provitamin A xantho-
phylls abound, and moreover it appears from current
research that both groups are essential to good vision
and perhaps to anticarcinogenesis.
In the twentieth century, pure white varieties of the
major cereals have been bred to meet market expecta-
tions by selecting for poor expression of the enzymes
of the carotenoid biosynthetic pathway, but older
varieties and landraces exist, so that breeders could, if
required, “turn the clock back.”
The germplasm resources are such that it should
be possible for breeders to produce, by conventional
means, cereals with sufficient provitamin A and
other essential carotenoids to satisfy the daily require-
ments of resource-poor people whose diet is severely
restricted in other sources of these nutrients
Among the three micronutrients—iron, zinc, and
carotenoids (deficiencies of which are major global
public health issues currently)—there are important
synergies in absorption, transport, and function that
strongly indicate substantial benefits to enhancing
all three nutrients together. The genetic resources to
meet this challenge are available and are not beyond
a moderately well-funded breeding programme for
TABLE 1. Provitamin A content of corn (mg/kg) calculated
from the contents of β-carotene + β-zeacarotene + cryptox-
anthin, presented as the means of six high- and six low-
carotene inbreds, and of the means of nine single crosses
made within each group [22]
Parental carotene Single High–low
concentration Selfeda crosses single cross
High 6.5 7.5 4.1
Low 1.3 1.7
a. Selfed refers to a variety crossed with itself.
Carotenoids in staple foods
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