Natural genetic variation for improving crop quality
Alisdair R Fernie1, Yaakov Tadmor2 and Dani Zamir3
The narrow genetic basis of many crops combined with
restrictions on the commercial use of genetically modified
plants, has led to a surge of interest in exploring natural
biodiversity as a source of novel alleles to improve the
productivity, adaptation, quality and nutritional value of crops.
Genetic methodologies have been applied to natural variation
to improve quality aspects that are associated with the
chemical composition of agricultural products. A future
challenge in this emerging field is to integrate metabolic,
phenotypic and genomic databases to allow a wider view of the
plant metabolome and the application of this knowledge within
genomics-assisted breeding.
Addresses
1
Abteilung Willmitzer, Max-Planck-Institut für Molekulare
Pflanzenphysiologie, Am Mühlenberg 1, 14476 Golm, Germany
2
Institute of Field and Vegetable Crops, Newe Ya’ar Research Center,
Agricultural Research Organization, PO Box 1021, Ramat Yishay,
30095, Israel
3
The Institute of Plant Sciences and Genetics in Agriculture, Faculty
of Agriculture, The Hebrew University of Jerusalem, PO Box 12,
Rehovot, 76100, Israel
Corresponding author: Zamir, Dani ([email protected])
Current Opinion in Plant Biology 2006, 9:196–202
This review comes from a themed issue on
Plant biotechnology
Edited by John Salmeron and Luis R Herrera-Estrella
Available online 15th February 2006
1369-5266/$ – see front matter
# 2006 Elsevier Ltd. All rights reserved.
DOI 10.1016/j.pbi.2006.01.010
Introduction
The improvement of crop species has been a fundamental
human pursuit since cultivation began. As a result of
genetic bottlenecks imposed during early domestication
and modern breeding activities, cultivated varieties carry
only a fraction of the variation present in the gene pool.
Wild ancestors of most crop plants can still be found in
their natural habitats and germplasm centres have been
established to collect and conserve these resources [1].
The development of molecular-marker techniques has
assisted in the introgression of defined genes or genomic
regions from wild species and landraces. To date, the
majority of such studies have focussed on improving crop
yield and disease resistance, but recent medical research
has highlighted the importance of crop compositional
quality for human health [2,3]; thus, this research field
is of rapidly increasing importance. An additional reason
Current Opinion in Plant Biology 2006, 9:196–202
for the renewed interest in biodiversity breeding results
from public concern about the use of genetically modification (GM) technologies, which hampers the chances of
such manipulated crops reaching certain markets. In the
past two decades, however, a vast research effort has been
expended on transgenic approaches for the metabolic
engineering of plants (recently reviewed [4]). In this
review, we do not dwell on GM and other mutagenic
approaches for metabolically engineering plants but rather
discuss classical genetic concepts for improved crop quality that are based on natural biodiversity. The majority of
this article is focussed on, although not limited to, tomato
(Solanum lycopersicum) because of the large number of
biochemical studies already carried out on this crop. We
conclude with a brief discussion on the relative merits of
introgression breeding and describe the impact that ‘network thinking’ will probably have on this research field.
Exotic introgression breeding
The potential of wild species as a source for genetic
variation to bring about crop improvement was recognized
early in the twentieth century [5,6,7]. Initial interspecific
breeding attempts met with severe problems, including
cross incompatibility between the wild species and cultivated crop; F1-hybrid sterility; infertility of the segregating
generations; reduced recombination between the chromosomes of the two species; and tight linkage between genes
that have negative effects and the traits of interest. Despite
these difficulties, there are many examples in which wild
introgression breeding has made a considerable contribution to the development of modern-day varieties [6,7].
Landraces are the earliest form of cultivars available to us
and represent the first steps in the domestication process.
In comparison to modern-day cultivars, landraces are
highly heterogeneous as they were selected for subsistence agricultural environments while uniformity was not a
major selection criterion. Early landrace varieties and wild
species provide a broad representation of the natural
variation that occurs in the species as a whole. The study
of such natural variation is being used increasingly both in
crop species [8–13] and in the model species Arabidopsis
thaliana [14,15] to facilitate gene discovery and to develop
both ecological and evolutionary perspectives of gene
function. In addition, broad-scale genomics efforts
have begun to utilize such genetic resources to survey
the level of phenotypic variance available within species
[14,16,17,18], with a view to developing strategies for
plant improvement.
Although exotic germplasm has been extensively
exploited as a source for monogenic traits, relatively little
work has been carried out on the complex traits that are
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Natural genetic variation for improving crop quality Fernie, Tadmor and Zamir 197
influenced by quantitative trait loci (QTL). Traits such as
yield, compositional quality and stress resistance show
complex inheritance patterns that result from the segregation of numerous interacting QTL, the expression of
which is modified by the environment [7]. One approach
to simplifying the analysis of complex traits is to use
introgression lines (ILs), which are a set of lines each
carrying a single defined chromosome segment from an
exotic genome in an elite genetic background. In recent
years, fruit from ILs of tomato, in particular Solanum
pennellii lines, have been evaluated for a relatively wide
range of traits, including morphological, transcriptional
and compositional traits [19–21], and serve as an important
example of the power of the introgression approach. Similar populations have been developed containing introgressions of other wild Solanum species (S. lycopersicoides [22];
S. habrochaites, S. neorickii and S. pimpinelifollium [23]; S.
sitiens [24]; S. peruviavum [25]; S. chmielewskii [26]; and S.
cheesmaniae [27]) into modern cultivars. There are also
exotic libraries of wild species introgressions into other
crop species, including rice, barley, soybean and pepper
[9–13]. Moreover, analogous approaches have been used in
mammalian systems; several different populations of congenic or chromosomal substitution strains of mice have
been generated and genotyped [28].
It is much easier to identify genomic regions that are
significantly associated with quantitative traits in IL
resources than in populations (such as recombinant
inbreds) that segregate simultaneously for multiple
QTL that are scattered throughout the genome
[23,28]. Such QTL often mask the effects of one
another by generating high variances in statistical analyses and by introducing an epistatic component. By
contrast, permanent nearly isogenic IL populations are
identical for their entire genome except for a single
introgressed region and, as a result, all of their phenotypic
variation is associated with the introduced segment.
[30] demonstrated that by pyramiding three independent yield-promoting genomic regions from the droughttolerant S. pennellii, they were able to elevate tomato yield
dramatically. In their study, these authors demonstrated
that the yields of hybrids that were parented by the
pyramided genotypes were more than 50% higher than
that of a control market-leader variety under both wet and
dry field conditions. In the rice example, QTL pyramiding that combined loci for grain number and plant height
in the same genetic background generated lines that
exhibited both beneficial traits [35]. Although only the
tomato example has, as yet, been confirmed under conditions of environmental stress, these examples clearly
highlight the potential of this approach for the biotechnological improvement of crop yield and stability [36].
Quality traits: chemical composition
The nutritional status of crop plants is ultimately dependent on their metabolic composition [37,38]. Nevertheless, while traits associated with yield and resistance have
been the focus of much research, quality traits that are
dependent on chemical composition are less well studied.
That said, there are some notable exceptions to this
statement, such as carotenoid content in tomato [39],
protein content in maize [40], and starch content in
potato and rice [41]. Moreover, seed soluble oligosaccharides, phytate, phosphate and cationic mineral content
have all been measured across a wide range of Arabidopsis
ecotypes [42]. Lastly, broad-range metabolite analyses
have been performed across the species of tomato that can
be readily crossed with the elite cultivated species, S.
lycopersicum [17], as well as across a wide variety of S.
lycopersicum cultivars [3,43]. In the following sections, we
document progress in understanding the genetic factors
that underlie metabolite composition by presenting
examples of successful manipulations of various chemical
classes in crops.
Protein, starch, cell wall and oil
Plant traits: yield and stress resistance
While it is our intention to concentrate largely on compositional quality traits, several exemplary studies have
been carried out in which the introgression of wild species
alleles into cultivated crop species have resulted in dramatic increases in yield [29,30,31] or in biotic and
abiotic stress resistance [32–34]. Several key findings
concerning the genetics of crop yield have been made
in recent years, covering a wide range of species including
tomato, rice, barley, soybean and pepper [9–13,30,31]. A
recent study in rice identified the QTL Gn1a, which
increases grain productivity and encodes a cytokinin
oxidase/dehydrogenase (OsCKX2), an enzyme that
degrades the phytohormone cytokinin. Reduced expression of OsCKX2 results in the accumulation of cytokinin
in inflorescence meristems, resulting in an increased
number of reproductive organs and enhanced grain yield
[35]. Using a combinatorial approach, Gur and Zamir
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Perhaps the best place to start this discussion is to
describe the Illinois long-term selection experiment for
protein and oil content in maize, which began in 1896.
This experiment is arguably the longest continuous
genetic experiment in higher plants. It comprises of over
100 cycles of selection, producing nine related populations that exhibit phenotypic extremes for grain composition and correlated traits [40]. The Illinois Selection
Strains span the known phenotypic extremes for maize
kernel composition (normally 8–12% protein and 4–6%
oil), which demonstrates the power of long-term selection
and the variation available within an old open-pollinated
variety for altering the expression of complex traits.
Selection responses of both protein and oil are greater
than 20 standard deviations from the original population
mean in the positive direction and four standard deviations in the negative direction [40]. The Illinois longterm selection lines are still used as a source of favourable
Current Opinion in Plant Biology 2006, 9:196–202
198 Plant biotechnology
alleles that are associated with oil, protein and starch
accumulation. Owing to space limitations, it is impossible
to document all of the other examples of improved
protein and oil content, so here we limit the discussion
to only a couple of recent examples. In the case of protein,
introgression of a high-grain-protein QTL from wild
emmer wheat, Triticum dicoccoides, markedly improved
the quality of pasta made from flour of wheat carrying
the QTL [44]. QTL for oil content have been discovered
in many species, including sunflower, soybean, rapeseed,
pea, oat and maize (see, for example, [45]). Similarly, the
genetic basis of both starch accumulation and starch
structure, which is important for industrial uses of the
biopolymer, have been the subject of extensive investigation in potato [46] and cereal species [41].
A further example of the use of the genetic approach to
study storage carbon metabolism was provided by the
recent study of Hazen et al. [47]. These authors determined the cell wall composition of maize pericarp in a
recombinant inbred line population, identifying QTL for
the xylose, arabinose, galactose and glucose content of the
cell wall. Analysis of the syntenic regions of the
sequenced rice genome identified strong candidate genes
that influence the monomeric composition of the cell
wall. Given the broad physiological importance of the
cell wall [48], it appears likely that this cereal study could
provide a basis for the analysis of the functional significance of cell wall composition across a range of biological
processes. As the cell wall is also an important source of
fibre in the diet, such studies could reasonably be anticipated to allow the improvement of crop yield and compositional quality.
Soluble carbohydrates
The contents of soluble carbohydrates are an important
determinant of crop quality from both calorific and taste
perspectives. In view of this fact, and the relative ease of
quantification of these compounds, it is perhaps unsurprising that many QTL studies that assessed sugar composition have been performed across a wide range of crop
species (recently reviewed in [49,50]). For the purpose of
illustration, we concentrate on studies carried out on the
tomato fruit. The fruit of wild tomato species display
considerable variation in sugar content [17]; a fact that
was exploited by the introgression of the sucrose accumulator gene (sucr) from S. chmielewskii into S. lycopersicum
[51]. This dramatically changed the ratio of sucrose to
hexose in the fruit. Similarly, research effort has been
placed on determining genetic factors that are responsible
for glucose to fructose ratios in fruits. This is of applied
interest since fructose is twice as sweet as sucrose, which
is sweeter than glucose. A QTL for glucose to fructose
ratios in fruits has been determined in advance backcross
populations of S. lycopersicum S. habrochaites crosses
[52], but the functional identity of the fructose glucose ratio
( fgr) locus remains to be identified.
Current Opinion in Plant Biology 2006, 9:196–202
QTL for sugar content have been identified in a wide
range of species, including potato, tomato, melon and
sugarcane (see [53] for a recent example). Recently one of
these, a moderate tomato QTL for Brix (total soluble
solids content), of which sugars and acids represent the
major constituents, was mapped to the cell wall invertase
gene LIN5. Subsequent high-resolution studies, using a
range of introgressions from different wild germplasm,
delineated this trait to a quantitative trait nucleotide
(QTN) that conferred altered kinetic properties to the
enzyme [23]. Physiological studies of the S. pennellii
introgression line that harbours this trait revealed that the
increased Brix in the ripe fruit was due to an increase in
sucrose and glucose, and demonstrated that enhanced
invertase activity in the fruit columella led to a greater
capacity to take up sucrose from the phloem [53]. This
example highlights the power of resolution of IL populations, as well as the potential that the introgression of
alleles from wild species has on the compositional
improvement of crops. Despite this fact, there are several
important questions that remain unanswered. For example, we do not understand the mechanisms that underlie
other sugar or Brix QTL in tomato, and we do not know
the extent of generality of the invertase finding in other
crop species. First steps have been made in addressing
the first issue. Many sugar/Brix QTL have been defined
in tomato fruit, and 63 genes that are putatively involved
in carbon metabolism have been mapped [19]. This
information, when taken in combination with transcriptional profiling of selected introgression lines along a
developmental time series [20], has facilitated the identification of candidate genes that underlie sugar/Brix
content. Similarly, recent observations in other crop species allow us to address the second question of QTL
conservation across taxonomic groups. A recent study in
potato revealed that the orthologous potato gene invGE
co-localises with cold-sweetening QTL Sug9. DNA variation at invGE, and its duplicated copy invGF, were
analyzed in 188 tetraploid potato cultivars, which had
previously been assessed for chip quality and tuber starch
content. This study resulted in the identification of two
closely correlated invertase alleles, invGE-f and invGF-d,
that are associated with better chip quality [54], suggesting that the cell wall invertase could be of general
importance for crop quality.
Organic and amino acids
In contrast to the work on soluble and storage carbohydrates, the manipulation of organic and amino acid content using wide crosses has received relatively little direct
attention. An example of the utilization of exotic variation
to affect fruit acidity comes from a recent study in melons
(Cucumis melo), where sweet varieties are characterized by
a low organic acid content. This is in contrast to practically
all other fruits in which fruit acidity, and especially the
sugar/acid ratio, is an indicator of fruit quality. High-acid
melons do not accumulate the high levels of sugar that are
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Natural genetic variation for improving crop quality Fernie, Tadmor and Zamir 199
characteristic of the sweet melon groups, and the combination of high sugar and high acid has not been reported
in C. melo. A single recessive gene determines high-sugar
accumulation in C. melo fruits and high acidity is controlled by a single dominant gene [55]. The combination
of increased acidity and high sugar provides the melons
with a unique taste because they have a sugar-to-acid ratio
not found in any sweet melon cultivars. Moreover, a
handful of studies in tomato and peach have addressed
the genetics behind these key components of taste
[56,57,58]. It should also be noted that the organic
acids, and possibly also glutamate, form major constituents of the total soluble solid or Brix trait described above.
More direct studies identified QTL for titratable acidity,
pH and citrate and malate content. Recently, such studies
have been integrated with taste analyses by trained
panels, which identified the glutamate/sugar ratio as an
important component of the flavour of tomatoes [56,57].
Vitamins, pigments and antioxidants
Vitamins, pigments and antioxidants have received much
research attention, particularly in highly coloured, genetically tractable crops such as tomato, peach and melon
[59]. This research was initially driven by the desire to
have attractive looking foodstuffs; however, research in
the medical field now suggests that pigments such as
lycopene in addition to vitamins confer health benefits to
the consumer [2]. Moreover, recent studies have indicated that fruit carotenoid pigments are precursors of the
norisoprenoids aroma compounds, which are derived from
the oxidative cleavage of carotenoids [60]. In recent years,
rice has been engineered by the introduction of three
genes of the carotenoid biosynthetic pathway to produce
relatively high levels (2 mg/g) of provitamin A [61]. The
production of ‘Golden Rice’ has rightly been hailed as of
great importance because it is estimated that vitamin A
deficiency leads to 1–2 million deaths each year. In
tomato, a wild-species-derived dominant allele has been
identified that increases b-carotene in the fruit as a result
of greater b-cyclase activity during fruit maturation. Fruit
that contain this allele have 100-fold greater b-carotene
content than Golden Rice [62]. This suggests that
resource investment in public nutritional education and
a breeding program of varieties that are rich in b-carotene,
and that are adapted to locations in which Vitamin A
deficiency is prevalent, would be highly prudent.
Moving on to the study of vitamins and antioxidants per se,
relatively little has been achieved to date, with most
studies concentrated on Vitamins C and E [21,63], glutathione [64], and total phenolic contents [21]. In all of
these studies, QTL were identified for enhanced metabolite content, suggesting that the manipulation of these
compounds by the introgression of beneficial alleles is
feasible. In tomato, QTL for vitamin C, and 15 genes that
encode enzymes that are involved in its synthesis and
metabolism have recently been mapped [65]. This work
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provides important information for co-localisation studies
involving QTL for this trait. In the case of tomato
pigmentation, the S. pennellii introgression lines defined
above were analysed with respect to carotenoid and
lycopene content. On the basis of trials in different
environments, 16 QTL that modified the intensity of
the red colour of ripe fruit were mapped. Candidate
sequences that are associated with the carotenoid biosynthesis pathway explained only a small portion of the
continuous variation in fruit colour [39]. Although the
studies described above suggest that the use of alleles
from wild species is a potentially important strategy for
elevating the levels of valuable compounds in food crops,
much work remains to be done. A more widespread
adoption of liquid chromatography-mass spectrometry
(LC-MS)-based methods of metabolite analysis [38] to
study breeding populations is one approach that has
excellent potential to expand our knowledge of the
genetic factors that underlie the accumulation of metabolites that are nutritionally beneficial.
Volatiles
As discussed above, the flavour of many fruits is highly
dependent on sugar and acid contents, and also on their
sugar:acid ratio. The correlation between consumer judgements and fruit and vegetables flavour is, however,
relatively weak, a fact that justifies the study of volatile
composition. A gas chromatography (GC)-MS-based
study quantified almost 400 volatile compounds in tomato
[66], but extensive research has only been carried out on a
handful of these. Utilizing a recombinant inbred line
population, generated from an intraspecific cross between
a cherry tomato line that has a good overall aroma intensity and an inbred line with a common taste but with
bigger fruit, allowed the identification of major QTL for
six aroma volatiles [67]. To date, however, the exact
mechanisms underlying these traits remain unresolved.
Intriguingly, a broader analysis recently revealed that
carotenoid pigmentation in both tomato and watermelon
fruits affected their volatile composition. Lycopene-containing fruit displayed greater contents of non-cyclic
norisoprenoids, such as geranial and neral, than fruit that
did not contain lycopene [59].
The detection of malodorous, a wild species allele that
affects tomato aroma, allowed the identification of a QTL
that is linked with a markedly undesirable flavour within
the S. pennellii introgression lines [68]. This trait corresponded to a 60-fold increase in phenylethanol and phenylacetaldehyde when compared to the cultivated
variety, providing a genetic explanation for one of the
aroma changes that occurred during domestication. The
above examples highlight the importance of wild germplasm for agronomic application and in improving our
fundamental understanding of metabolic pathway structure and regulation, but it is also a great resource for
assessing trait evolution.
Current Opinion in Plant Biology 2006, 9:196–202
200 Plant biotechnology
Conclusions
The study of natural variation has brought great advances
in our understanding of plant morphology and the
response of plants to biotic and abiotic stresses. The
application of sophisticated analytical tools has begun
to extend the utility of such genetic material in helping
us to understand and ultimately improve crop compositional quality. The examples presented here represent
the first steps in this direction. They demonstrate that the
modification of quantitative traits, including extreme
phenotypic or compositional changes in the fruit or kernel
that often cannot be achieved through mutagenesis or
transgenic approaches is available through access to wide
genetic variation. The use of molecular-marker-assisted
breeding is clearly a feasible alternative to GM technology, particularly given the public concern over the use of
GM crops. Our review demonstrates that suitable genetic
material, such as ILs, must be developed for the efficient
exploration and utilization of exotic variation. A further
advantage of permanent IL populations is that phenotyping can be carried out at many different levels and
laboratories, allowing a more comprehensive analysis of
the molecular networks that underlie crop quality. An
example of the wider view provided by an integrative
approach comes from tomato (N Schauer, Y Semel, D
Zamir, AR Fernie, unpublished). To identify components
of fruit metabolic composition, we phenotyped the S.
pennellii ILs for 75 metabolites and 10 yield-associated
traits. More than 1000 QTL were identified, revealing
that at least 50% of the variation in fruit metabolic profiles
was associated with plant morphology. Thus, it is important to note that only part of the metabolic variation is
regulated by genes that are involved directly in the
biochemical pathway. Given that transcript-profiling platforms are rapidly becoming available for an ever wider
range of crop species, that proteomic and metabolite
profiling platforms are essentially species-independent
[69], and that similar projects are underway in several
crop species [70–72], the identification of QTL that are
linked to certain profiles is likely to prove highly informative in providing a more holistic view of the mechanisms that underlie crop compositional quality.
Acknowledgements
Research in our laboratories was supported by the Deutsche
Forschungsgemeinschaft, the Bundesmisterium für Bildung und
Forschung, and the Max-Planck Gesellschaft (A.R.F.), the ‘ARO
Center for the Improvement of Cucurbit Fruit Quality’ (Y.T.) and a
collaborative grant to A.F. and D.Z. from the German–Israeli
Cooperation Project (DIP).
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