Genetic approaches to reducing losses of stored grain to
insects and diseases
David Bergvinson and Silverio Garcı́a-Lara
Insects and diseases devour or damage a fifth or more of stored
food grains each year in many parts of the world. Modern
breeding and genomics promise progress in characterizing the
resistance to the pests responsible for these losses that is
present in the vast and diverse gene pool of cereals, as well as
advances in incorporating this resistance into productive and
acceptable crop varieties. The impact of such varieties could
be dramatic in developing countries, where grain infestations
are most common and harmful, and where surging populations
require affordable food.
Addresses
International Maize and Wheat Improvement Center, Apdo. Postal
6-641, 06600 Mexico DF, Mexico
e-mail: d.bergvinson@cgiar.org
Current Opinion in Plant Biology 2004, 7:480–485
Available online 19th May 2004
1369-5266/$ – see front matter
ß 2004 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2004.05.001
Abbreviations
GE genetic engineering
HPR host-plant resistance
LDC less-developed country
QTL quantitative trail locus/loci
Introduction
By the end of the next two decades, the world will have
to feed approximately 2.5 billion more people with
less arable land, fewer renewable and non-renewable
resources, and fewer farmers. This challenge emerges
against a backdrop of rapid urbanization, climate change,
globalization, and fluctuating grain prices, especially in
the less-developed countries (LDCs) where the popula-
tion growth will be concentrated. Conversely, the rate of
production gains for staple food crops resulting from
conventional breeding has slowed in LDCs from 2.9%
each year (during the Green Revolution era in the 1960s)
to 1.9%, with gains frequently being offset by environ-
mental stresses and declining soil fertility [1].
One way to increase the quantity and quality of food grain
is to reduce damage from insects and diseases that attack
stored grain. Such damage is commonly responsible for
losses of more than 20% of the grain harvested in LDCs,
where tropical conditions allow insects and disease agents
to reproduce rapidly and to colonize unprotected grain
[2]. Complex expert systems [3] that use models for
Current Opinion in Plant Biology 2004, 7:480–485
germination, respiration, molds and the risk of pest infes-
tation help to maintain grain quality in developed coun-
tries, but are unavailable in most LDCs. Given the
expense of such systems, the development of host-plant
resistance (HPR) to storage pests and diseases is an
attractive option. The most successful avenue for disse-
minating agricultural technology has been improved
germplasm, which has reached farmers even in areas
where extension services are weak.
This discussion focuses on cereals, with most examples
being drawn from maize (Zea mays L.), on which con-
siderable HPR research is currently being conducted.
Advances in understanding the biochemical and genetic
bases of HPR are key to this work.
Development of genetic variation for storage
pest and disease resistance
Genetic variation for HPR encodes a suite of survival
traits that have evolved in plants over millions of years.
Farmers, especially small-scale farmers, have selected
directly or indirectly for traits of interest, including
HPR for storage pests [4]. Some traits that provide
HPR against the pests and diseases of harvested crops
have been selected against, however, to facilitate harvest-
ing and processing. Primitive maize, for example, may
have resulted from a cross between a perennial teosinte
(Zea diploperennnis) and eastern gamagrass (Tripsacum
dactyloides), giving rise to a hybrid whose hard fruitcase
inhibited oviposition by the maize weevil (Sitophilus
zeamais [Motsch.]) [5]. Over time, the hard fruitcase
was selected against but functionally replaced by protec-
tive leaf sheaths (i.e. the husk), which constitute the
kernel’s first line of defense against pests and pathogens.
The domestication of other crops similarly involved
selection for traits that enhanced production, processing
and storage, while some variation in traits that are asso-
ciated with storage pest resistance was maintained [6].
This genetic diversity [7] can now be exploited to char-
acterize resistance mechanisms that are associated with
different crops, and to incorporate resistance into
improved varieties using conventional [8] and genetic
engineering (GE) approaches [9].
The genetic composition of the different tissues within
the seed is a key consideration in large grain crops such as
maize. The testa (pericarp) is completely maternal (2n);
the endosperm and aleurone are 3n (2n female, 1n male);
and the embryo equally represents both parents (2n). As a
result, in analyses of whole seed, the endosperm will
dilute pericarp tissue [10], thereby masking pericarp
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 Reducing losses of stored grain Bergvinson and Garcı́a-Lara 481

biochemicals that are associated with resistance. These
considerations now figure in genetic [11] and biochemical
analyses [10,12] of HPR.
Increasing the resolution of our genetic
understanding of resistance
Molecular mapping and proteomics are now being
applied to improve our understanding of and to manip-
ulate HPR. Molecular maps have been developed for
Fusarium moniliforme [13], and for Aspergillus flavus and its
associated alfatoxin B1 [14,15]. The phenotypic variation
that could be accounted for by 3–10 quantitative trait loci
(QTL) in each mapping population was low, ranging from
just 10 to 25%. QTL x environment interactions were
significant for major QTL, making it difficult to imple-
ment a marker-assisted selection program using markers
linked to these QTL.
Proteomics has much to contribute in this work. A com-
prehensive study of alfatoxin-resistant maize employed
an analysis of peptide-sequence homology to identify
proteins that are associated with alfatoxin resistance
[16]. Several of the associated genes are also involved
in tolerance of heat and drought, environmental stresses
that influence the production of alfatoxin [17].
Molecular maps for resistance to maize weevil have
recently been developed (S Garcı́a-Lara, DJ Bergvinson,
Abstract 154, 56th Maize Genetics Meeting, 11–14 March
2004, DF Mexico). QTL for maize weevil resistance, like
those for resistance to fungi, explain only a small propor-
tion of phenotypic variation, totaling just 25% over seven
QTL. However, these QTL map to regions of the maize
genome that are associated with the production of cell
wall biochemicals, such as cellulose synthase (CesA5 and
CesA6) [18], pericarp cell wall sugars (arabinose and
galactose) [12], fiber [19], cellulose and p-coumaric acid
[20]. Given the close association between QTL for weevil
resistance and cell wall components in maize, it seems
possible that fortification of the pericarp cell wall through
marker-assisted selection could deliver enhanced resis-
tance to storage pests.
Biochemical and biophysical bases
for resistance
Researchers addressing HPR against storage pests and
diseases in food crops face the imposing challenge of
enhancing resistance while maintaining the desired nutri-
tional and processing qualities of the grain. For example,
resistance biochemicals, such as soluble phenolics in
sorghum [21], may result in an unpleasant grain flavor.
Potentially toxic or allergenic biochemicals will require
extensive testing before their contents in food or feed can
be increased [22]. Two less problematic avenues from a
food-safety perspective are, first, physical barriers that do
not adversely affect processing (e.g. fiber and waxes [23]),
and second, biochemicals that have very specific and
localized activity against storage pests and diseases but
are not toxic or unpalatable to humans or livestock.
Specific components of grain that have been reported
to confer resistance to insects or diseases are briefly
discussed below and are summarized in Table 1.
Phenolic acids
Hydroxycinnamic acids and their derivatives are ubiqui-
tous in the plant kingdom in both soluble and bound
forms, and have roles in cell wall structure and defense in
cereals. The soluble form of phenolics and phenolic

Table 1

Biochemical factors in cereals that are associated with resistance to storage pests and diseases.

Biochemical group Components Mode of actiona Localization Activity Reference

Hydroxycinnamic Phenolic acid amides Antibiosis Concentrated in aleurone layer Maize weevil [10]
acids Fusariumspp. [24]
CW simple phenolics Antibiosis and structural Embryo and aleurone Maize weevil [6]
Fusariumspp. [25]
CW diferulates Structural Pericarp Fusariumspp. [27]
Oxidative products Antibiosis Whole grain Several pathogens [34]
and insects
Structural proteins Extensins Structural or bind to Concentrated in pericarp Fusarium spp. [31]
pathogen
Protein inhibitors Amylase inhibitor Antibiosis Whole grain Fusariumspp. [35]
Maize insects [36]
Trypsin inhibitor Antibiosis Whole grain Wheat pathogens [37]
Rice insects [9]
Ribosomal inhibitors Ribosomal inactivation Antibiosis Aleurone layer Several pathogens [52]
protein (RIP)
Waxes C18-C26 hydrocarbons Antibiosis Outer layer of seed Aspergillus flavus [23]
Enzymes Peroxidase Antibiosis Whole grain Wheat pathogens [33]
Maize insects [34]
Storage proteins Globulin Antibiosis Whole grain (endosperm) Several pathogens [16]
a
Antibiosis is a resistance mechanism that has an adverse effect on the invading organism. CW, cell wall.

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482 Commentary
amines have been reported to reduce both fungal and
insect attacks in grain [6,24,25]. Phenolic amines inhibit
glutamate-dependent neuron receptors in insects [26],
but fortunately this class of compounds is localized in the
aleurone layer [10].
Cell wall bound phenolic acids play an integral role in the
assembly of structurally diverse polysaccharides, struc-
tural proteins, phenolic compounds, and other materials
that serve many functions in cell walls. Phenolic acids
help to strengthen cell walls in grasses, thereby protecting
against insect and fungal invasion [6,27]. Microspec-
trophotometric scans of maize kernel cross-sections
(Figure 1b) show that cell wall phenolics are concentrated
largely in the embryo and pericarp. Closer examination
using autofluorescence microscopy (Figure 1c) points to
their localization in the pericarp. Figure 1d illustrates
how different forms of linkage interact to increase the
mechanical strength of the pericarp [28]. Ferulic acid
bound to heteroxylans can covalently link heteroxylans
through the peroxidase-mediated formation of diferulic
acids (Figure 1d) and, to a lesser extent, via cycloaddition
reactions in the presence of UV light that form truxillic
and truxinic acids [29].
Recent evidence suggests that diferulic acids are pro-
duced in the Golgi cisternae and exported to the plasma
membrane [30]. Using this model, Fry et al. [30] predict
that increased cross-linking limits cell growth rates when
the activity of cell wall peroxidase is high. Pathogen-
induced oxidative bursts would probably increase difer-
ulate production as part of a defense response [30].
Recent studies show that the concentration of diferulate
is 10-fold higher in the pericarp than in vegetative tissues
(DJ Bergvinson, unpublished), supporting its role in dis-
ease resistance [27].
Hydroxyproline-rich glycoproteins
Hydroxyproline-rich glycoproteins (HRGP), or extensins,
are localized in the pericarp and are highly correlated with
fungal resistance [31]. HRGPs genes have been most
studied in dicots [32] and are thought to have a helical
structure and a rod-like shape. Extensins are bound to the
cell wall complex (Figure 1d) through covalent linkages
by isodityrosine between extensins, to pectins or pheno-
lic-polysaccharides by cross-linking with feruloylated
sugars, or through oxidization of extensins (Val, Pro,
Lys) by peroxidase to form stable protein–protein
cross-links [32].
Peroxidases and protein inhibitors and as potential
sources of resistance
Grain peroxidases catalyze the polymerization of phenolic
acids and HPRP in protective tissues such as the pericarp,
thereby limiting fungal [27,33] and insect invasion [34].
The protease inhibitors, such as a-amylase for fungi
[35] and insects [36] and trypsin inhibitors for insects
Current Opinion in Plant Biology 2004, 7:480–485
Figure 1
(a) (b)
(c) Pericarp Embryo
Aleurone
Endosperm
(d)
1 Cellulose microfibrils
5
6
2 Lignin
4
Structural
proteins
Heteroxylans
3
3
7
Current Opinion in Plant Biology
Cell wall components that are associated with maize weevil resistance in
maize. (a) Adults emerge through the pericarp after completing
development inside the kernel. (b) Microspectrophotometric scan
using a 365/418-nm florescence filter to estimate phenolic acid
concentrations in a cross-section of the maize kernel (same
orientation as that in (a)). Phenolic acids are localized in the pericarp and
embryo of cereals. (c) Autofluorescence of phenolic acids is
concentrated in the pericarp and aleurone of maize. (Scale bar
represents 100 mm.) (d) Model of the pericarp cell wall. Structural
proteins, namely extensins, may (1) surround cellulose microfibrils, (2)
link with other structural proteins by isodityrosine bridges, (3) link to
feruloylated heteroxylans or (4) intercalate with heteroxylans. (5)
Hemicellulose, formed mostly of heteroxylans, is covalently linked by
dehydrodiferulic acids but (6) ferulic-acid moieties may also link to
lignin. (7) Cellulose microfibrils may be associated by hydrogen bonding
with hemicellulose that has little or no branching. Based on [29].
[9] and fungi [36,37], form another protein group that has
received considerable attention. These inhibitors are
found mainly in the endosperm of several crops and
inhibit protein degradation by invading insects and fungi.
Breeding for resistance
Breeding for HPR requires an integrated team of ento-
mologists, pathologists, breeders, molecular biologists,
nutritionists, and social scientists to ensure that products
are effective, safe, and meet consumer demands. Figure 2
gives an overview of the breeding process, which will vary
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 Reducing losses of stored grain Bergvinson and Garcı́a-Lara 483

Figure 2 Once a donor for acceptable resistance alleles has been

found, the trait is ready for movement into commercial
Develop an ecologically
varieties. The most effective strategy is the combined use
relevant, large-scale of molecular markers and conventional breeding/screen-
screening technique ing, in proportions that will depend on the inheritance of
the trait, the availability and cost of markers, and the
Screen germplasm amount of donor DNA that is acceptable for the target
for resistance:
Novel gene product Lines/varieties
genotype [41]. In general, molecular markers have facili-
from different species Populations tated the successful conversion of lines by movement of
Accessions one or two alleles, including a single recessive allele
Related species
(opaque2 [o2]) in maize, to improve grain quality [42].
Characterize For additive or quantitative traits, such as resistance
resistance
mechanism
against maize weevil, population improvement using
conventional breeding and selection techniques have
Is the trait viable when food safety, processing,
and consumer acceptance are considered? been effective [8,43].
No Yes
Review/revise screening Characterize Increasing interest in the in-situ conservation of crop
technique and screen inheritance genetic resources has resulted in several approaches in
germplasm or search for which farmers participate to foster this conservation
new novel genes
[44]. A new approach called ‘targeted allele introgression’
Dominant Additive
Use molecular Population is being used to introduce storage pest and disease
markers to move improvement and resistance into farmers’ varieties, while preserving the
resistance alleles line recycling to varieties’ food and processing qualities and enhancing
or novel genes develop varieties their genetic diversity (DJ Bergvinson, unpublished).
into commercial with improved
varieties resistance
Genetically engineered crops
The use of GE to develop novel crop varieties in
Commercial varieties with improved industrial countries has engendered heated debate con-
resistance to storage pests and cerning the risks and benefits of these varieties. Most
diseases
investment in GE is in industrialized countries, but
Current Opinion in Plant Biology
three developing countries have made significant pub-
lic investments in biotechnology: Brazil (US$ 2 mil-
A simplified breeding strategy for the development of varieties that are
resistant to storage pests and diseases. Ideally, the development of lion), China (US$ 112 million), and India (US$ 15
resistant varieties should be integrated with breeding programs aimed million) [45]. Recent studies suggest that small-scale
at developing grains with enhanced nutritional quality. farmers in developing countries stand to benefit more
from the use of GE to develop novel varieties that have
improved plant protection than do commercial farmers
considerably depending on breeding objectives and in industrial countries [46]. This is because farmers in
constraints. The first step is to develop a screening developing countries have limited access to agrochem-
methodology that is ecologically relevant for the target icals and suffer greater losses from insect pests and
organism(s) and that provides high-throughput potential. diseases [46].

Germplasm screening should start by examining ad-
vanced lines or commercial varieties already available
to farmers. If no resistant genotype is found, then more
genetically diverse germplasm sources, such as popula-
tions, genebank accessions, or wide-crosses, should be
explored to access alleles that are not present in cultivated
crop species [5–7].
Once sources of resistance are found, the biochemical
basis for the resistance should be elucidated and analyzed
to ensure its acceptability to consumers and safety for use
in food and feed. Protein-based resistance mechanisms, in
particular, may be allergenic [38–40]. If a trait fails to
meet food safety criteria, then new sources of resistance
must be sought.
Genetic engineering holds considerable promise, but
must be evaluated in a comparative framework alongside
conventional technologies [47]. In addition, the poten-
tial impact of genetically engineered crops in centers of
origin of genetic diversity, for example, the impact of
growing GE maize in Mexico, still requires considerable
study [48]. The first transgene that provided effective
control of several storage pests is that encoding avidin, a
glycoprotein derived from the chicken egg that seques-
ters the vitamin biotin [49]. Because it binds biotin,
however, avidin that is not denatured by processing
(i.e. heat) would pose a nutritional risk to humans and
livestock who consume large quantities of grain contain-
ing it. The transformation of rice with the a-amylase
gene from maize to control storage pests of rice [9] is

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484 Commentary
particularly promising, given that this class of inhibitor
does on appear to pose a threat to human health or
nutrition [36].
Will resistance to storage pests and
diseases compromise grain or
nutritional quality?
This is a relevant question when consumer preferences,
and the different resistance mechanisms and their
potential impact on processing quality, are considered.
Ideally, grain quality and resistance to storage pests
should be developed in parallel so that consumers rea-
lize the full nutritional benefit of a crop. Protein quality
can be improved through GE by increasing the content
of lysine, an essential amino acid, through modification
of the anticodon for tRNAlys [50] or through the use of
RNA-interference to enable the dominant expression of
recessive mutants (e.g. o2) to increase lysine content
[51]. Provided these events do not alter the grain tex-
ture, they could be combined with conventional sources
of resistance [6,8,15] or with GE-derived resistance [9]
to provide nutritious varieties that can be stored by
farmers, especially those who depend on cereals for
subsistence.
Conclusions
Reducing post-harvest storage losses through genetic
improvement is both feasible and urgently needed to
meet food demands in coming decades. A small but
noticeable renaissance in the use of resistant varieties
to minimize storage losses is taking place, especially in
those ecologies where infrastructure for storage does not
exist. To capitalize on genetic diversity for storage pest
resistance, researchers have made significant progress in
understanding the biochemical, biophysical, and genetic
bases of HPR, which is essential to ensure that the traits
being selected meet with consumer demands. Traits that
meet these criteria are now being mapped to confirm their
role in resistance and to identify candidate genes using
sequence homologies and proteomics. The introgression
of resistance alleles from the same crop species, using
marker-assisted selection or GE, will probably meet with
greater public acceptance and possibly require less rig-
orous testing to document food safety than will the
introduction of genetic material from other species.
The real potential of this technology will be felt most
in LDCs because the technology is packaged in the seed
and should be designed to ensure that farmers have the
option to recycle seed, a common practice for subsistence
farmers.
Acknowledgements
We apologize to those whose work could not be covered because of
space limitations. We thank Mike Listman for reviewing the manuscript.
Financial support for post-harvest research from the Canadian
International Development Agency and the Syngenta Foundation for
Sustainable Agriculture is gratefully acknowledged.
Current Opinion in Plant Biology 2004, 7:480–485
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