Journal of Experimental Botany, Vol. 66, No. 5 pp. 1145–1156, 2015
doi:10.1093/jxb/eru473 Advance Access publication 26 November 2014
Darwin Review
Effects of abiotic stress and crop management on cereal
grain composition: implications for food quality and safety
Nigel G. Halford1,*, Tanya Y. Curtis1, Zhiwei Chen2 and Jianhua Huang2,*
1 Plant Biology and Crop Science Department, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK
Biotechnology Research Institute, Shanghai Academy of Agricultural Sciences, 2901 Beidi Road, Minhang District, Shanghai 201106,
Peoples Republic of China
2 * To whom correspondence should be addressed. E-mail: [email protected] or [email protected]
Received 23 September 2014; Revised 24 October 2014; Accepted 28 October 2014
Abstract
The effects of abiotic stresses and crop management on cereal grain composition are reviewed, focusing on phytochemicals, vitamins, fibre, protein, free amino acids, sugars, and oils. These effects are discussed in the context of
nutritional and processing quality and the potential for formation of processing contaminants, such as acrylamide,
furan, hydroxymethylfurfuryl, and trans fatty acids. The implications of climate change for cereal grain quality and
food safety are considered. It is concluded that the identification of specific environmental stresses that affect grain
composition in ways that have implications for food quality and safety and how these stresses interact with genetic
factors and will be affected by climate change needs more investigation. Plant researchers and breeders are encouraged to address the issue of processing contaminants or risk appearing out of touch with major end-users in the food
industry, and not to overlook the effects of environmental stresses and crop management on crop composition, quality, and safety as they strive to increase yield.
Key words: Climate change, crop nutrition, drought, food safety, food security, grain composition, heat stress, processing
contaminants, regulatory compliance.
Introduction
The ability of crops to tolerate abiotic stresses such as an
excessive or inadequate supply of water, high winds, extreme
temperatures, frost, salt, and other osmotic stresses is a key
aspect of yield resilience, and its improvement has long been
a target for plant breeders. The issue now has more resonance
than ever because of the anticipated effects of climate change,
which is predicted by the International Panel for Climate
Change to bring about a rise in temperature of up to 5 °C
by the end of this century and an increase in the frequency
and severity of extreme weather events (Stocker et al., 2013),
potentially affecting crop yields, farmer earnings, reliability
of the food supply, food quality, and food safety (Vermeulen
et al., 2012; Curtis and Halford, 2014).
The severe droughts experienced in Australia in 2006–
2007 and Russia in 2010 may be portents of such events.
Both resulted in spikes in crop commodity prices (Curtis
and Halford, 2014) because both Australia and Russia are
major wheat exporters in normal years. The hike in food
prices in 2008 was a tipping point in the west, with policymakers finally accepting that the food security that had been
enjoyed for several decades could not be taken for granted.
There has also been concern over the potential impact of
climate change on food security in the world’s most populous country, China (see, for example, Xiong et al., 2007
2010; Wang et al., 2009; Zhang et al., 2010). This concern
has increased recently following a period of extreme heat
and drought in the south of the country in 2013. Figure 1
shows yellowing of rice plants brought about by severe
drought and heat in a field trial at Shanghai Academy of
Agricultural Sciences in 2013, and the leaf rolling and white
spike phenotype caused by drought stress in Hainan province in 2010.
© The Author 2014. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved.
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1146 | Halford et al.
Phytochemicals, vitamins, and dietary fibre
Fig. 1. Top: upland rice growing in a field trial at Shanghai Academy
of Agricultural Sciences, Shanghai, China during a period of extreme
temperature and drought in August 2013. Bottom: rice grown in a farm of
Hainan province (China) in 2010, showing the leaf rolling and white spike
phenotypes brought about by drought stress (kindly provided by Professor
Hanwei Mei, Shanghai Agrobiological Gene Centre).
Clearly, improving crop yield per se and making it more
resilient to stress will be crucial to ensuring food security
in the coming decades. However, yield is not the only crop
parameter affected by abiotic stress, and the impact of
stress and, by implication, climate change on crop composition is also important. The composition (quality) of a
crop product affects its processing properties and the nutritional value, flavour, colour, and aroma of the food that is
produced from it. Crucially, it also affects food safety and
regulatory compliance, with the potential for formation of
undesirable contaminants such as acrylamide, furan and
related products, and trans fatty acids being determined by
the composition of the raw crop product. Composition is
also affected by crop management, notably plant nutrition,
with management factors interacting with the effects of the
environment.
Here we focus on the world’s major grain crops and review
how cereal grain composition is affected by abiotic stress
and crop management, and we consider the implications
this has for food quality, processing, safety, and regulatory
compliance.
Cereal products are deeply embedded in the dietary culture of many countries. They are a rich source of energy, as
well as fibre, protein, B vitamins, iron, calcium, phosphoric
acid, zinc, potassium, and magnesium (Nyström et al., 2008;
Shewry, 2009). While all cereal grains contain valuable minerals, vitamins, and phytochemicals (defined as non-nutritive
plant chemicals that are believed to have protective or disease-preventive properties), there is considerable variation
between species and genotypes. The European Union FP6
HEALTHGRAIN diversity programme, for example, analysed 150 bread wheat (Triticum aestivum) lines and 50 other
lines of spelt (Triticum spelta), emmer wheat (Triticum dicoccum), einkorn wheat (Triticum monococcum), oats (Avena
sativa), rye (Secale cereale), and barley (Hordeum vulgare),
and found significant differences in levels of dietary fibre and
phytochemicals that are considered to have health benefits
(Ward et al., 2008). The study identified a number of wheat
lines that combined high levels of phytochemicals and fibre
with good yield and processing quality, leading the authors to
conclude that it would be possible for plant breeders to adopt
phytochemical and fibre content as breeding targets. There is
little indication that this has occurred yet, possibly because
breeders and the food industry are unconvinced that increasing the levels of beneficial components that are already present in a food would add value to their products. However,
commercial decisions such as this one are outside of the control of scientists.
Subsequent analysis of 26 of the wheat cultivars grown
in six site×year combinations spread across Hungary, the
UK, Poland, and France in 2006 and 2007 showed important effects of the environment on nutritional value, with all
groups of phytochemicals apart from alkylresorcinols and
bound phenolic acids showing strong positive correlations
with the mean temperature between heading and harvest
(Shewry et al., 2010). Folates and free phenolic acids also
showed negative correlations with total rainfall during the
same period, while stanols expressed as a percentage of total
sterols also showed positive correlations with temperature
and negative correlations with rainfall. The amount of waterextractable arabinoxylan, a major component of dietary fibre
in wheat grain, on the other hand, correlated negatively with
temperature and positively with rainfall in both the bran and
white flour fractions.
Li et al. (2009) also examined the relative contribution of
genotype and environment to variation in arabinoxylan content, in this case of 25 hard winter and 25 hard spring wheat
varieties grown in three different environments across the
north-west of the USA. They concluded that both the total
arabinoxylan content of the grain and the distribution of
arabinoxylans between water-soluble and -insoluble fractions
could be highly influenced by the environment, although
there were also clear genetic effects and gene×environment
interactions.
Rakszegi et al. (2014) studied the effects of both heat and
drought stress during grain development on the dietary fibre
content and composition (arabinoxylan and β-glucan) in
Effects of abiotic stress and crop management on grain composition | 1147
three winter wheat varieties. Both stresses reduced β-glucan
content of the grain but increased protein and arabinoxylan
content, except that drought stress decreased arabinoxylan
content in a drought-tolerant variety, Plainsman V.
Barley grain is also a rich source of dietary fibre, but
β-glucan rather than arabinoxylan is the predominant component, accounting for ~70% of the dietary fibre in the barley
starchy endosperm (white flour fraction). β-Glucan content
has been shown to be affected by nitrogen application and
water availability in barley in a study conducted in Turkey
(Güler, 2003). Generally, high nitrogen levels increased grain
β-glucan content, while higher levels of irrigation tended to
decrease it, in contrast to its effects on β-glucan in wheat grain
reported by Rakszegi et al. (2014). Narasimhalu et al. (1995)
also studied the effect of environment on β-glucan content
of barley grain, this time in Canada, using 75 different cultivars and six different sites across the country. Environment,
represented by the different sites, significantly affected total
β-glucan content, with grain from barley grown in the drier
east containing more β-glucan than grain produced in the
west. Similarly, Swanston et al. (1997) found more β-glucan in
grain from barley grown in Spain compared with barley from
the considerably cooler and wetter environment of Scotland,
UK. These results were at odds with those of a previous study
that suggested that low glucan content occurred in grain from
drier environments (Coles et al., 1991). Other factors may
have been at play to explain the contrasting results, but at
least it can be concluded that β-glucan, and therefore dietary
fibre content of barley grain, is sensitive to environmental
conditions.
Brown rice is also a valuable source of phytochemicals and
vitamins. Indeed, it was the work of doctors in Asia in the late
19th century, investigating the effect of incorporating brown
rice into the diets of prisoners and livestock for preventing
the disease beriberi, that led to the discovery that foods contain complex nutrients that are essential for health. Prisoners
and animals fed a diet of white rice were prone to developing the disease, which affects the peripheral nervous system,
while those fed brown rice were not (Carpeneter, 2000). This
eventually led to the coining of the word vitamin and the discovery of thiamine (vitamin B1). Brown rice also provides
lipid-soluble antioxidants, including ferulated phytosterols
such as γ-oryzanol, tocopherols, and tocotrienols. Elevated
temperatures during cultivation have been shown to change
the profile of some of these phytochemicals, for example
increasing α-tocotrienol and/or α-tocopherol while decreasing γ-tocopherol and γ-tocotrienol (Britz et al., 2007).
This section of the review brings home the contribution
that cereal products, particularly wholegrain cereal products, make to our diet and food security, in terms of providing nutritious as well as sufficient food. It is particularly
important to make this point at the moment because some
clinicians and dieticians have suggested that cereal, and particularly wheat, consumption contributes to overeating and
obesity (see, for example, Davis, 2011). This notion has been
debunked by Brouns et al. (2013), who instead found associations between the consumption of the recommended amounts
of wholegrain wheat products and significant reductions in
risk for type 2 diabetes, heart disease, and weight gain. The
other conclusion from this section is that if we value the vitamins, phytochemicals, and dietary fibre present in wholegrain
cereals then more should be done to understand the effect
of environmental and crop management factors on their
concentration.
It is a fact, however, that persuading consumers to eat more
wholegrain cereal products in preference to foods produced
from white flour has not proved easy, and while the consumption of brown rice may have significant health benefits compared with white rice, the husk is discarded not just because
of consumer preference but also because it rapidly goes rancid during storage, especially in tropical countries.
Protein
Protein content and composition is an important determinant
of cereal grain quality and it is sensitive to drought and heat
stress as well as atmospheric CO2 concentration. Heat stress,
for example, reduces starch deposition in wheat grain, resulting in an increase in grain protein content (Wardlaw et al.,
2002; Gooding et al., 2003). Wrigley et al. (1994) showed
that it also affects protein composition and that, as a consequence, wheat dough strength is adversely affected by even
a short period of high temperature (> 35 °C) during grain
filling. The reduction in dough strength is associated with a
decrease in the proportion of insoluble glutenin to soluble
gliadin proteins in the grain (a higher proportion of glutenins
promotes cross-linking between proteins in gluten, the proteinaceous matrix that gives wheat dough its viscoelasticity)
(Blumenthal et al., 1993). The effect of the high temperature
is greater if it occurs during mid to late grain filling than if it
occurs early (Corbellini et al., 1997), while slightly lower temperatures, ~30 °C, are actually beneficial, giving better dough
strength than lower temperatures (Wrigley et al., 1994). Balla
et al. (2011) showed that drought stress also causes a disproportionate reduction in the glutenin fraction compared with
the gliadin fraction in wheat grain, with an adverse effect on
dough strength. Drought stress has also been shown to cause
a small reduction in total protein content in two maize cultivars grown in Pakistan (Ali et al., 2010) but to increase it by
up to a fifth in rice (Crusciol et al., 2008; Fofana et al., 2010).
Temperature stress, on the other hand, causes a reduction in
protein content in rice (Ziska et al., 1997).
Elevated levels of atmospheric CO2 (700 ppm compared
with 350 ppm) have been shown to have a negative effect on
wheat grain quality, largely through reducing the overall protein content, although increased CO2 does increase grain yield
(Blumenthal et al., 1996). Grain grown under elevated CO2
produces poorer dough and decreased loaf volume, which is
important given that the atmospheric CO2 concentration has
already risen from a pre-industrial level of 270 ppm to almost
400 ppm and is rising at 1–2 ppm per year, taking it to levels
not seen for 20 million years.
Wheat protein content and quality are also affected by
plant nutrition and therefore crop management. The importance of a plentiful supply of nitrogen to produce a high yield
of grain with not only a high protein content but also protein
1148 | Halford et al.
quality that is acceptable to bread-makers has been known
since the 19th century (see Hawkesford, 2014, for a recent
review). Also important for protein quality is an adequate supply of sulphur. Zhao et al. (1999), for example, showed that
sulphur deficiency limits storage protein accumulation, with
wheat grown in sulphur-deficient soil favourably accumulating sulphur-poor proteins at the expense of sulphur-rich glutenins. Indeed, in that study, sulphur was shown to be more
important for bread-making quality than nitrogen. This confirmed a much earlier study that found barley plants to have
reduced ability to synthesize sulphur-rich storage proteins
(called hordeins in barley) when starved of sulphur (Shewry
et al., 1983). The total hordein fraction was decreased from
51% to 27% of the seed nitrogen in one variety and from 46%
to 26% in another. Different combinations of nitrogen and
sulphur fertilizer have also been shown to affect grain quality in durum wheat (Lerner et al., 2006; Rogers et al., 2006;
Godfrey et al., 2010).
The changes in accumulation of different types of protein in cereal grain in response to nutrition can be attributed to changes in gene expression. Seed storage protein
gene expression is controlled primarily at the transcriptional
level (Bartels and Thompson, 1986; Sørensen et al., 1989)
and responds sensitively to the availability of nitrogen and
sulphur in the grain (Giese and Hopp, 1984; Duffus and
Cochrane, 1992). Many wheat, barley, and rye storage protein
genes contain a so-called GCN4-like motif (GLM), nitrogen element, or N motif (reviewed by Shewry et al., 2003),
nucleotide sequence G(A/G)TGAGTCAT, in the promoter
region. This motif exerts a negative effect on gene expression
at low nitrogen levels but a positive one when nitrogen levels are adequate (Müller and Knudsen, 1993), and binds at
least two different transcription factors (Hammond-Kosack
et al., 1993; Albani et al., 1997). However, little is known
about the mechanisms by which storage protein gene expression responds to sulphur.
While considering the importance of grain proteins for
quality, it should be remembered that for small subsets of
the population the proteins of wheat, rye, and barley have
an adverse effect on health (reviewed by Shewry, 2009). Some
are allergenic, for example, with the respiratory allergy, bakers’ asthma, being an important occupational allergy affecting bakers. Many proteins appear to be involved (reviewed
by Tatham and Shewry, 2008), but the most important are a
class of α-amylase inhibitors known as CM proteins because
of their solubility in chloroform/methanol mixtures. Wheat
also causes food allergies, including wheat-dependent exercise-induced anaphylaxis (WDEIA), in which consumption
of wheat followed by physical exercise can induce an anaphylactic response. The proteins responsible are a group of
seed storage proteins known as ω5-gliadins (Tatham and
Shewry, 2008; Shewry, 2009). Dietary intolerance to wheat
is also an important problem, with coeliac disease, a chronic
inflammation of the bowel that reduces the bowel’s ability to
absorb nutrients, affecting ~1% of the population of Western
Europe, and dermatitis herpetiformis, which causes skin
eruptions, affecting between 0.2% and 0.5% of the population (Shewry, 2009). These conditions are triggered by a wide
range of gluten proteins, so there appears to be little scope
for addressing the problem through either breeding or crop
management.
Free amino acid and sugar accumulation
Free amino acids are sometimes overlooked when considering
grain concentration because most of the nitrogen in the grain
is incorporated into proteins. This is unfortunate because, as
we describe below, free amino acids, together with sugars, are
major determinants of processing quality and in some cases
food safety. Free amino acids are always present in plant tissues to enable protein synthesis to proceed. They accumulate
to high concentrations during some developmental processes
such as germination and senescence, but even higher concentrations can occur in almost any tissue in response to a range
of both biotic and abiotic stresses, including nutrient deficiency, pathogen attack, toxic metals, drought, and salt stress
(reviewed by Lea and Azevedo, 2007).
Examples of this in cereals include the accumulation of free
amino acids in the leaves of Hordeum species in response to
salt stress, which was demonstrated in a study by Garthwaite
et al. (2005). This study showed that concentrations of glycinebetaine (an N-trimethylated amino acid), asparagine, and
proline all increased in leaves with increased external NaCl
concentration. The proline increase differed between species;
H. vulgare, for example, had a 17-fold increase in the expanding leaf blade, while H. muratum had an 8-fold increase.
A similar increase in free amino acids was also observed
during leaf folding for drought-stressed pearl millet plants
(Kusaka et al., 2005). The levels of free asparagine and proline were increased 9- and 18-fold, respectively, 6 d after stopping irrigation, and 15- and 28-fold after 9 d. The excess of
asparagine in the leaves was considered to be an indication of
protein degradation under stress conditions, but could have
arisen in part through de novo synthesis.
The increase in concentration of some amino acids and
their derivatives in vegetative tissues in response to osmotic
stress imposed by, for example, drought and salt, has led to the
hypothesis that increases in the concentration of these metabolites are not just symptoms of stress but are an important
part of the stress response, decreasing cell osmotic potential
and thereby increasing turgor while decreasing plant water
potential. It follows that increased tolerance to stress could be
imparted by genetic interventions that increase the concentration of these metabolites, with proline and glycinebetaine
receiving particular attention. This has been reviewed in detail
by Lawlor (2013). Examples of this approach being applied
to cereals include the overexpression of a Δ1-pyrroline-5carboxylate synthetase from mothbean (Vigna aconitifolia L.)
under the control of a stress-inducible promoter in transgenic
rice (Zhu et al., 1998), leading to increased proline accumulation. Second-generation transgenic plants expressing the
transgene showed increased biomass compared with controls
under both salt and drought stress. A mothbean Δ1-pyrroline5-carboxylate synthetase has also been overexpressed in
wheat, again under the control of a stress-inducible promoter
Effects of abiotic stress and crop management on grain composition | 1149
(Vendruscuolo et al., 2007), resulting in improved drought
tolerance, although this was mainly due to reduced oxidative
stress rather than osmotic adjustment. Lightfoot et al. (2007)
targeted another area of amino acid metabolism by overexpressing a bacterial glutamate dehydrogenase gene in transgenic maize. The plants showed improved drought tolerance,
leading the authors to conclude that transgenic plants overexpressing glutamate dehydrogenase could outperform their
conventional counterparts in semi-arid conditions.
Lawlor (2013) expressed scepticism over whether transgenic plants such as these show genuinely improved drought
tolerance, as opposed to changes in growth, development, or
metabolism that give the appearance of improved drought
tolerance but would not bring about better performance of
the crop under drought conditions in the field. Nevertheless,
it is an approach that continues to be adopted by many
researchers.
Proline concentration in vegetative tissues may be the target of most genetic interventions like these, but, as we state
above, proline is not the only free amino acid that accumulates in response to stress. The free asparagine concentration
is also highly responsive to environmental conditions and,
crucially for grain quality and food safety, while it usually
accounts for <10% of the total free amino acids in cereal
grains (Lea et al., 2007), it can become by far and away the
predominant free amino acid in the grain under stress conditions. In general, free asparagine accumulates when the rates
of protein synthesis are low and there is a plentiful supply
of reduced nitrogen (Lea et al., 2007), either as a result of
inhibition of protein synthesis or through direct effects on
asparagine metabolism, or both. Not surprisingly, therefore,
nitrogen availability correlates positively with free asparagine content and this has been shown in barley (Winkler and
Schön, 1980), wheat (Martinek et al., 2009), and rye (Postles
et al., 2013). When there is a plentiful supply of nitrogen,
deficiencies in other minerals become important (reviewed by
Lea et al., 2007). Sulphur deficiency in particular can cause a
massive (up to 30-fold) increase in the accumulation of free
asparagine (up to 50% of the total free amino acid pool) and
to a lesser extent free glutamine in wheat, barley, and maize
(Shewry et al., 1983; Baudet et al., 1986; Muttucumaru et al.,
2006; Granvogl et al., 2007; Curtis et al., 2009), although rye
is much less responsive, at least under field conditions (Postles
et al., 2013).
As described in the section on proteins, sulphur deficiency
brings about a reduction in the expression of sulphur-rich
storage proteins in wheat and barley, and this may explain
some of the increase in free amino acid accumulation in the
grain. However, the fact that free asparagine and to a lesser
extent free glutamine are disproportionately accumulated
compared with other free amino acids suggests that these
amino acids are used by the plant to store nitrogen under
nutrient-limited conditions. Consistent with this hypothesis, asparagine synthetase gene expression in wheat has
been shown to increase under sulphur-limited growth conditions. This response appears to involve the protein kinase,
TaGCN2 (Byrne et al., 2012); TaGCN2 is related to General
Control Non-derepressible 2 (GCN2), a master regulator
of amino acid metabolism and protein synthesis in yeast
(Saccharomyces cerevisiae) (Wek et al., 1989). GCN2 and
TaGCN2 phosphorylate the α-subunit of translation initiation factor 2 (eIF2α). In yeast this results in translational
up-regulation of a transcription factor, GCN4. There is no
clear homologue of GCN4 in plants, but, as discussed in the
section on proteins, some storage protein genes do contain
a regulatory motif that matches the GCN4 binding site. It
is therefore possible that TaGCN2 could link the regulation
of storage protein and asparagine synthesis, although much
more of the signalling systems involved would have to be elucidated before that could be confirmed.
Asparagine synthetase gene expression in wheat also
increases in response to salt and osmotic stress (Wang et al.,
2005), and there is evidence from several studies that the free
asparagine concentration in the grain of both wheat and
rye varies considerably in the same variety grown at different locations or in different years, showing that asparagine
metabolism is responsive to multiple environmental and crop
management factors (Taeymans et al., 2004; Baker et al.,
2006; Claus et al., 2006a; Curtis et al., 2009, 2010).
The same is true for sugar concentrations in cereal grain.
While significant genotypic variation has been reported
in studies on, for example, wheat (Claus et al., 2006a;
Muttucumaru et al., 2006; Hamlet et al., 2008) and rye
(Curtis et al., 2010; Postles et al., 2013), environmental factors are also important. For example, high temperatures
during grain filling in wheat cause an increase in sucrose,
reducing sugars, and sugar phosphates, and a reduction in
starch (Jenner, 1991). Gooding et al. (2003) also reported a
decrease in Hagberg falling number, which is indicative of
reduced starch and increased sugars, in heat-stressed wheat.
Curtis et al. (2010) analysed a diverse selection of rye varieties, including some that are no longer used in cultivation,
grown at sites in France, Hungary, Poland, and the UK over
several growing seasons, and reported a wide range of sugar
concentrations, particularly for sucrose (26.81–49.52 mmol
kg–1), across the different sites and harvest years, even within
the same genotype in some cases. Postles et al. (2013) also
measured sugar concentrations in rye, but in this case the
grain came from elite commercial varieties grown in a field
trial at a single location over one growing season, and a lower
and much tighter range of concentrations was obtained (4.39–
5.03 mmol kg–1 for sucrose). The two studies also showed
differences in reducing sugar concentration, with glucose
being the most abundant reducing sugar in the 2010 study,
again showing a considerable range, from 0.64 mmol kg–1
to 33.43 mmol kg–1, and fructose being the most abundant
reducing sugar in the 2013 study, ranging from 2.88 mmol
kg–1 to 4.37 mmol kg–1.
Postles et al. (2013) also looked at the effect of nitrogen
and sulphur nutrition on sugar levels in rye grain. Nitrogen
affected the fructose, glucose, and total reducing sugar concentration, but the effect was variety-dependent, with one
variety, Agronom, for example, accumulating a higher concentration of reducing sugars at an intermediate nitrogen
application rate (100 kg ha–1) than at very low or high application rates, while another, Askari, had a lower concentration
1150 | Halford et al.
of reducing sugars at the intermediate nitrogen than at lower
or higher application rates. Sulphur had no effect on the
reducing sugars, but its application at 15 kg ha–1 or 40 kg ha–1
resulted in a significant reduction in sucrose concentration in
one variety, Rotari.
The results of these studies emphasize the effects of genotype, environmental conditions, including crop management,
and genotype×environment interactions on sugar concentrations in cereal grain. An even wider range of sucrose concentrations has been reported for maize (12.91–89.60 mmol
kg–1; Harrigan et al., 2007) and rice (15.10–58.60 mmol kg–1;
Smyth et al., 1986). However, relatively few studies have
investigated the effects of abiotic stress on sugar concentrations in cereal grain, while many have focused on the effect of
stresses on the sugar content of leaves and seedlings, a theme
that has characterized physiological studies of the effects of
stress and crop management on sugars in cereals and, indeed,
other crops. We have reviewed these studies in detail previously (Halford et al., 2011) and, since they are not directly relevant to this review, have not done so again here. In summary,
cereals and other plants interconvert monosaccharides, disaccharides, and more complex carbohydrates such as fructan in
order to cope with osmotic stresses, including those caused
by salt, freezing, and drought, as well as other stresses such as
hypoxia and early senescence (Halford et al., 2011). Indeed,
rye’s superior stress tolerance compared with its near relatives
is attributed to a greater capacity for carbohydrate storage
and more rapid hydrolysis of fructan to increase concentrations of simple sugars when required. Interestingly, fructan
has recently been shown to accumulate in the early stages of
wheat grain development (Verspreet et al., 2013), although its
role in that case is not known.
Colour, flavour, and aroma volatiles and processing
contaminants produced from sugars and free
amino acids
Understanding the role of sugars and free amino acids, and
the interconversion of simple sugars and complex, insoluble
carbohydrates in vegetative tissues in response to osmotic
and other stresses is important for the development of
genetic interventions that will make crops more resilient to
and therefore higher yielding under abiotic stress conditions.
However, it is also important to understand the effects that
abiotic stress has on the concentration of these metabolites in
the grain because free amino acids and sugars have profound
effects on the processing properties of the grain. Indeed, free
amino acids and sugars have been considered in the same section of this review because they combine during baking, frying, and high-temperature processing to produce a host of
compounds, including some imparting colour, flavour, and
aroma, and others that are potentially harmful to health.
The reaction in which free amino acids and sugars combine to form these compounds is the Maillard reaction, an
umbrella term for a series of non-enzymic reactions that
takes place only at high temperatures. The reaction requires a
reducing sugar such as glucose, fructose, or maltose, and the
products of the reaction include melanoidin pigments and
a complex mixture of compounds that impart flavour and
aroma, including pyrazines, pyrroles, furan (which can also
be described as a contaminant), oxazoles, thiazoles, and thiophenes (Mottram, 2007). The most important bread flavour
compound, for example, is 6-acetyl-1,2,3,4-tetrahydroxypyridine, while 2-acetyl-1-proline provides the main flavour in
wheat and rice crackers. So, it is the Maillard reaction that
gives bread crust, biscuits, rye crisp-breads, and a wide variety of other popular foods their characteristic flavour, aroma,
and texture.
The Maillard reaction is very complex, and is described
in detail elsewhere (Nursten, 2005; Mottram, 2007; Halford
et al., 2011; Curtis et al., 2014b). While many of its products are highly desirable, some are not (Friedman, 2005) and
can be classed as processing contaminants; that is, substances
that are produced in a food when it is cooked or processed,
are not present or are present at much lower concentrations in
the raw, unprocessed food, and are undesirable either because
they have an adverse effect on product quality or because they
are potentially harmful (Curtis et al., 2014b). This definition
distinguishes them from substances such as mycotoxins that
are biotic in origin and, while important, are outside the
scope of this review.
Products of the Maillard reaction in cereal products that
can be considered as processing contaminants include acrylamide and furan (Curtis et al., 2014b) (Fig. 2). Of these,
acrylamide is probably the one that is of most concern to the
food industry at present. Acrylamide is formed within the
Maillard reaction when free asparagine participates in the
later stages (Mottram et al., 2002; Stadler et al., 2002; Zyzak
et al., 2003). Indeed, the carbon skeleton of the acrylamide
that forms is derived entirely from asparagine. It should be
noted, however, that while this appears to be the major route
for acrylamide formation, others have been proposed, for
example with 3-aminopropionamide as a possible transient
intermediate (Granvogl and Schieberle, 2006) or through
pyrolysis of gluten (Claus et al., 2006b). Nevertheless,
Fig. 2. Diagrams representing the structures of acrylamide, furan, and
hydroxymethylfurfuryl
Effects of abiotic stress and crop management on grain composition | 1151
asparagine concentration correlates closely with acrylamide
formation in heated wheat and rye flour (Muttucumaru et al.,
2006; Granvogl et al., 2007; Curtis et al., 2009 2010; Martinek
et al., 2009; Postles et al., 2013).
Acrylamide is familiar to biochemists because of its use
in gel electrophoresis, and it also has applications in wastewater treatment, papermaking, and manufacture of fabrics.
It has been classified as a Group 2A, ‘probably carcinogenic to humans’, chemical by the International Agency for
Research on Cancer (International Agency for Research on
Cancer, 1994) because of the carcinogenicity it has shown in
rodent toxicology studies (Friedman, 2003; Taeymans et al.,
2004). The concentrations of acrylamide in the human diet
are much lower than those used in such studies (Friedman,
2003), and the results of epidemiological studies on the effect
of dietary acrylamide on cancer rates in humans have been
inconsistent. Nevertheless, the latest report on the issue
from the European Food Safety Authority (EFSA)’s Expert
Panel on Contaminants in the Food Chain (CONTAM)
described acrylamide in food as potentially increasing the
risk of developing cancer for consumers in all age groups
(EFSA CONTAM Panel, 2014). The Food and Agriculture
Organization of the United Nations and the World Health
Organization (FAO/WHO) Joint Expert Committee on Food
Additives (JECFA) has also concluded that the presence of
acrylamide in the human diet is a concern (Joint FAO/WHO
Expert Committee on Food Additives, 2011). Acrylamide also
has neurological, reproductive, and developmental effects at
high doses, but CONTAM considers these not to be a concern at current levels of dietary exposure (EFSA CONTAM
Panel, 2014).
The European Commission issued ‘indicative’ levels for
acrylamide in food in early 2011, then revised them in 2013,
with levels for many cereal products being lowered (European
Commission, 2013). These values are intended to indicate
the levels that the Commission considers the food industry
should be able to achieve, based on the results of its acrylamide monitoring programme. In the USA, the Food and Drug
Administration (FDA) has not issued advice or restrictions,
but has developed an ‘action plan’ with a number of goals,
including identifying means to reduce exposure. However, in
2005, the Attorney General of the State of California filed a
lawsuit against four food companies for not putting a warning label on their products to make consumers aware that the
products contained acrylamide. The lawsuit was settled in
2008 when the companies committed to cutting the level of
acrylamide in their products to <275 μg kg–1 and paid US$3
million in fines.
Fried potato products and coffee are major contributors
to dietary acrylamide, but many cereal-based foods are also
affected, including bread, biscuits, breakfast cereals, crispbreads, cakes, pastries, and tortilla chips. More acrylamide
tends to form in products that are baked to a crisp texture
and dark colour, such as biscuits, crisp-breads, and breakfast
cereals: the most recent EFSA report puts the mean acrylamide content for biscuits and crisp-breads sampled in the
European Union at 265 μg kg–1 (parts per billion) (EFSA
CONTAM Panel, 2014) and for breakfast cereals at 161 μg
kg–1. However, dietary exposure is a function not only of the
concentration of acrylamide in the product but also of the
amount of the product that is consumed, and although the
acrylamide content of soft bread is comparatively low (mean
42 μg kg–1), soft bread is the major cereal-based contributor
to dietary intake, accounting for between 15% of total intake
in the UK and 42% in Germany (European Food Safety
Authority, 2011a).
The food industry reacted quickly to the discovery of
acrylamide in some of its products and has devised many
strategies for reducing acrylamide formation by modifying
food processing (compiled in a ‘Toolbox’ produced by Food
Drink Europe, 2011). However, the cereal breeding industry
generally did not react with the same urgency. So, while several studies have shown that there are significant differences
between varieties with respect to free asparagine concentration and therefore acrylamide-forming potential in the grain
(reviewed by Halford et al., 2012), there is no sign of low free
asparagine concentration being adopted as a major target by
most breeders or that varieties with high acrylamide-forming potential are being excluded from breeding programmes.
What is more, with most work on the issue being carried out
in Europe, where rice and maize are not major crops, there
is little information available on the acrylamide content of
rice and maize products that may contain acrylamide, such
as fried rice, rice crackers, and cakes (such as Chinese nian
gao) and maize tortillas and tortilla chips, and screening of
maize and rice varieties appears to be lacking altogether. In
this respect, cereal breeders appear to be out of touch with
the needs and priorities of the food industry that uses its
products. In contrast, some potato breeders have begun to
use acrylamide-forming potential in their advertising, which
at least indicates that they are taking the issue seriously.
Farmers also have a part to play. The effect of sulphur
deficiency on the concentration of free asparagine in wheat
and barley grain means that sulphur availability is the most
important factor affecting the acrylamide-forming potential
of these grains. In a recent study in the UK, for example,
acrylamide formation was analysed in flour from wheat grain
samples produced from six field trials in which different levels
of sulphur had been applied (Curtis et al., 2014a). The trials comprised four different varieties of winter wheat, grown
at three different locations over three harvest years, with five
different levels of sulphur fertilization. The level of application that gave a significant benefit compared with no sulphur
application, with no further significant benefit with higher
levels of application, ranged from 5 kg to 20 kg of sulphur
ha–1. However, application at the 20 kg sulphur ha–1 rate led
to significantly lower grain asparagine concentration and less
acrylamide formation compared with lower rates in two of
the trials, the results for one of which are shown in Fig. 3.
Given the necessity of preventing free asparagine accumulation in all conditions, it was concluded that sulphur-containing fertilizer should be applied at a rate of 20 kg sulphur ha–1
wherever sulphur deficiency is thought to be a risk and wheat
is being grown for use in products for human consumption.
This rate of sulphur application is at the top of the range
of rates of sulphur fertilizer already recommended in the
1152 | Halford et al.
Fig. 3. Free asparagine concentration in the grain and acrylamide
formation in wholemeal flour (heated for 20 min at 170 °C) for wheat cv.
Alchemy grown at Brockhampton, Herefordshire, UK in 2009–2010 with
different rates of sulphur application (data from Curtis et al., 2014a).
Fertiliser Manual (RB209) for wheat in the UK (Fertiliser
Manual, 2011). However, previous recommendations were
based on the rate of application required to ensure that the
protein quality of bread-making wheat was sufficient to meet
the requirements of bakers. Some food products with a relatively high risk of acrylamide formation, such as breakfast
cereals and biscuits, do not require wheat with the high quality protein content that is preferred for bread-making. The
results of the study showed that it is important that sulphur
be applied at a rate of 20 kg ha–1 to wheat destined for these
products as well as wheat being grown for bread production,
regardless of yield and other quality issues (Curtis et al.,
2014a).
As we have described above, nitrogen has the opposite effect
on free asparagine concentration to sulphur, with increasing nitrogen application bringing about an increase in free
asparagine concentration. Nitrogen fertilizer is, of course,
extremely important for obtaining high yields of good quality
grain, in any cereal. The current best advice is that the crop
should be supplied with other nutrients as well, particularly
sulphur, to ensure that as much of the nitrogen as possible
is incorporated into protein rather than accumulating as free
asparagine (Halford et al., 2012).
There are some things, of course, that farmers cannot control and, as we have stated earlier in this section, asparagine
metabolism is responsive to multiple environmental factors.
It is important that the exact environmental triggers for
asparagine accumulation in cereal grain are identified in the
interests of quality control and, in the longer term, the development of strategies for producing varieties that are consistently low in grain asparagine concentration across a range of
environments.
Acrylamide is not the only contaminant formed in the
Maillard reaction: furan (Fig. 2) and related compounds are
also Maillard reaction products and are attracting increasing
attention because of their potential effects on human health.
Furan consists of a five-membered aromatic ring comprising
four carbon atoms and one oxygen (Fig. 2). It is classed by
the International Agency for Research on Cancer as ‘possibly
carcinogenic’ to humans (Group 2B) (International Agency
for Research on Cancer, 1995), because it causes liver cancer
in rodents (Leopardi et al., 2010). Like acrylamide, the actual
risk posed by the presence of very low levels of furan in food
is not known. The Maillard reaction involving sugars and free
amino acids is not the only route for its production: it can
also form directly from the degradation of sugars, polyunsaturated fatty acids (PUFAs; which also feature in the next
section), or ascorbic acid (reviewed by Curtis et al., 2014b).
Cereal-based foods make a significant contribution to
dietary exposure to furan prior to adulthood. Cereal-based
baby foods, for example, contribute 3% of the dietary intake
in infants and 12% in toddlers, while other cereal products
contribute 7.7% of the dietary intake of older children and
10% of the intake of adolescents (European Food Safety
Authority, 2011b). In adults, however, dietary intake from
cereal products is dwarfed by that from coffee.
A related compound that can form in cereal products is
hydroxymethylfurfuryl (HMF) (Ramírez-Jiménez et al.,
2000), which consists of a furan ring with both aldehyde and
alcohol functional groups (Fig. 2). HMF arises via the dehydration of fructose (Román-Leshkov et al., 2006) and is a
common contaminant of dark beers (Husøy et al. 2008) and
over-cooked biscuits. Indeed, it is sometimes used as an indicator of excessive heat treatment in biscuit manufacture. This
is mainly because products containing high levels of HMF
may also contain a lot of acrylamide, so measuring HMF
levels is a quality control procedure that is used to ensure
that acrylamide levels are lower than the indicative value.
However, HMF itself may have safety implications because
one of its metabolic products is 5-sulphoxymethylfurfural,
which shows potential toxicity and carcinogenicity in rodent
studies (Husøy et al., 2008).
As with acrylamide, modifying food processing conditions
can reduce furan formation in foods (Fan et al., 2008), but
there appears to have been little work on reducing the furanforming potential of crop products, possibly because of the
multiple routes through which furan can form. Clearly, lowering fructose levels would be a possible strategy for reducing
HMF formation, but so far we are not aware of this being
investigated in a scientific study and it would almost certainly
also affect the production of beneficial Maillard reaction
products. Environmental factors are clearly also potentially
extremely important, given the changes in sugar concentration that can occur in response to abiotic stresses.
Oils
Most cereal grains do not contain enough oil to be considered suitable for commercial oil production, but maize and
oat grain contain ~5% and 7% oil, respectively. Oat oil is not
widely used in food or industrial processes, except as an ingredient in some cosmetics and skin moisturisers, but maize oil
is an important commodity, with 1.3 billion litres of it being
used in the USA alone in 2012, mostly for margarine and
cooking oil but more recently also for biodiesel production.
The principle components of plant oils are, of course, triacylglycerols, which are made up of three fatty acid molecules
Effects of abiotic stress and crop management on grain composition | 1153
esterified with glycerol. Different fatty acids are distinguished
by the length of their hydrocarbon chain and by the number
and position of double bonds between the carbon atoms in the
chain, with saturated fatty acids containing no double bonds,
monounsaturates a single double bond, and PUFAs multiple
double bonds. Maize oil is typically made up of ~12% palmitic
acid (saturated, 16-carbon chain, 0 double bonds, represented
as 16:0), 2% stearic acid (18:0), 30% oleic acid (18:1), 54% linoleic acid (18:2), and 1% α-linolenic acid (18:3), but Ali et al
(2010) showed that this changes dramatically in response to
drought stress, which not only causes a reduction in grain oil
content by 40% but also causes oleic acid to increase to >25%
of the total at the expense of linoleic acid.
PUFAs are relatively unstable because they are subject to
thermal oxidation during cooking and high-temperature processing, giving rise to lipid peroxides. Lipid peroxides form
polymers that give a dark coloration and may be toxic, and
can break down to form products that cause a rancid, ‘off’
flavour and odour, as well as furan, which was discussed in
the previous section. Oxidation also occurs during long-term
storage, so a high PUFA content shortens the shelf-life of the
oil. Food processors prevent PUFA oxidation by chemical
hydrogenation of the double bonds, producing a more stable,
saturated fatty acid. This may also be done to solidify the
oil, making it suitable for the production of margarines (saturated fatty acids have a higher melting point that unsaturated
fatty acids). The problem with chemical hydrogenation of
PUFAs is that some of the double bonds remain unsaturated
but change from the cis form, with the two hydrogen atoms
attached to the carbon atoms involved in the double bond
on the same side, to the trans form, with the two hydrogen
atoms on opposite sides. Trans fatty acids arising from partial hydrogenation of plant oils are now regarded as being as
harmful as saturated fatty acids when consumed (reviewed by
Brouwer et al., 2010), and can therefore be considered to be
another important class of processing contaminants.
The accumulation of more oleic acid and less linoleic acid
in maize under drought stress may produce a more stable oil
that does not require chemical hydrogenation. However, the
fact that the environmental conditions can have such a profound effect on the fatty acid profile is important and requires
further study. This also has implications for biodiesel production, which is now a major use for many plant oils. Biodiesel
is manufactured from plant oils by transesterification of
triacylglycerols with methanol, producing fatty acid methyl
esters (FAMEs) with glycerol as a by-product. The properties
of a particular biodiesel are therefore dependent on the composition of the plant oil from which it is made.
Conclusions
We have reviewed the effects of abiotic stress and crop management on the composition of cereal grain and the implications this has for food quality and safety. The need to ensure
that cereal crops have a sufficient supply of nutrients so that
the grain contains sufficient, good quality protein for highend uses such as bread-making is widely understood. What
has received less attention from cereal scientists and breeders
is the importance of grain composition for food safety. One
aspect in particular that needs much more investigation is the
identification of specific environmental stresses that affect
composition in ways that have implications for food safety
and how these stresses interact with genetic factors and will
be affected by climate change. This is a key conclusion of this
review.
It is important that this is addressed because the problem
of processing contaminants in cereal and other food products does not appear to be one that is going to go away any
time soon, and the food industry faces a difficult and evolving
regulatory system that has to be complied with regardless of
the inconsistencies in the raw materials that the industry has
to use. Indeed, the acrylamide problem is one of the most
pressing currently facing large sectors of the food industry.
Processors have put a lot of effort and money into reducing
the levels of acrylamide in their products to as low as is reasonably achievable without fundamentally changing the characteristics that define those products and are demanded by
consumers (the ALARA principle). There is increasing frustration within the food industry at the lack of engagement of
plant scientists and breeders when it is clear that the development of varieties that gave a more consistent raw material
would make it much easier for food producers to comply with
regulations. Plant researchers and breeders are therefore in
danger of appearing to be out of touch with major end-users.
It is also conceivable that plant breeders who continue to
ignore the issue will suffer in the marketplace. One of the
simplest and cheapest ways for a food company to address a
contaminants problem in one of its products is to switch to a
raw material with a lower risk of that contaminant forming,
whether it be a different variety or even in some cases a different crop species. The company can then continue to make its
product without costly changes to the manufacturing process.
It is in the interests of researchers in the plant sciences to
recognize the importance of the food industry as a potential
beneficiary of plant research. As a community, plant scientists argue that their role in underpinning a sustainable and
competitive agriculture industry justifies the support they
receive from taxpayers, but would do well to point out just
as strongly the relevance and importance of their work to
the food industry. The economic case for this in developed
countries is simple: the UK, for example, which is classed by
the World Bank as a high income country, has an efficient
and highly productive agriculture sector, but the sector’s gross
value added (GVA) figure (i.e. the total value of the goods
that it produces) of £7.7 billion per annum (Department for
Environment, Food and Rural Affairs, 2013) represents only
0.6% of the UK’s total, while the GVA of the food industry
is more than three times that at £24 billion (Food and Drink
Federation, 2014). Indeed, on the basis of its turnover of £92
billion and workforce of 400 000 people, the food industry
is the largest sector within UK manufacturing. Agriculture
continues to be a major contributor to the economy of developing economies, but its contribution tends to decline as the
economy develops. In China, for example, which is classed
as an upper middle income country, agriculture accounted
1154 | Halford et al.
for 15.1% of economic activity in 2000 but for only 10.1% in
2012 (OECD, 2014).
We conclude by encouraging researchers, breeders, and
farmers not to overlook the effects of environmental stresses
and crop management on crop composition in the drive to
increase yield, with a reminder that the FAO’s definition of
food security refers to safe and nutritious as well as sufficient food (Food and Agriculture Organization of the United
Nations, 2003).
Acknowledgements
NGH is supported via the 20:20 Wheat Programme at Rothamsted Research
by the Biotechnology and Biological Sciences Research Council (BBSRC)
of the UK. TYC was funded through BBSRC stand-alone LINK project
‘Genetic improvement of wheat to reduce the potential for acrylamide formation during processing’. Rothamsted Research receives grant-aided support from the BBSRC. ZC was supported as a visiting worker at Rothamsted
Research in 2011–2012 by an overseas visiting grant from Shanghai Academy
of Agricultural Sciences, Shanghai, Peoples Republic of China.
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