Plant Physiol, January 2001, Vol. 125, pp. 156-159
Changing Paradigms in Plant Breeding
Maarten
Koornneef* and
Piet
Stam
Laboratory of Genetics, Department of Plant Sciences, Graduate
School of Experimental Plant Sciences, Wageningen University,
Dreyenlaan 2, 6703 HA Wageningen, The Netherlands (M.K.); and
Laboratory of Plant Breeding, Department of Plant Sciences, Graduate
Schools of Experimental Plant Science and Production Ecology and
Resource Conservation, P.O. Box 386, Wageningen University, 6700 AJ
Wageningen, The Netherlands (P.S.)
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INTRODUCTION |
The origin of plant breeding
traces back to the dawn of agriculture and the domestication of plants,
when nomadic man first became a settler. This started in those regions
of the world where plants suitable for domestication, such as large
grain grasses, grew in the wild. We envisage that the early farmers
collected seeds and vegetative reproductive organs (tubers and bulbs)
and kept part of them for planting the next season's crop. During this
process, they selected naturally occurring variants that were higher
yielding and better adapted for cultivation. Selected variants would,
for instance, retain their seeds after ripening, have larger and
healthier seeds, and carry less thorns or prickles, resulting in what
we now sometimes refer to as the "domestication syndrome" of
cultivated plants. Uncontrolled hybridization in farmers' fields, as
well as with wild relatives and/or progenitors occurring in the natural
habitat, most likely increased the variation in the germplasm available
to early farmers. Over many centuries, the conscious or unconscious
selecting by farmers, along with selective pressures imposed by the
temporal and spatial heterogeneity of the growing conditions,
resulted in land races, genetically heterogeneous populations that are
locally adapted to the conditions imposed by man and the physical
environment. The process of crop improvement by farmers' selection,
however, was a very slow process compared with science-based
professional plant breeding.
The first gradual change toward plant breeding as a specialized
profession occurred when private agricuturalists began to deliberately
select cultivars and started selling seeds of improved quality. In
practice, this form of plant breeding implied the selection of superior
variants among existing variation (usually through mass selection and
occasionally through line or family selection) and increasing the
uniformity of the crop. Until the beginning of the 20th century,
controlled hybridization to create novel variation available for
selection was rarely involved.
The rediscovery of Mendel's work at the turn of the century
provided a solid scientific basis for plant breeding. The awareness of
the particulate nature of hereditary "factors" and the possibility to create novel combinations of traits by making crosses contributed enormously to the professional "seedmanship" of the 20th century.
Concepts such as resistance breeding, the introgression of specific
traits (often disease resistances) from less-related and often
difficult-to-cross species, mutation breeding, hybrid and synthetic
varieties, the use of male sterility, and incompatibility to enable the
efficient production of such hybrid varieties all emerged before 1975. These developments were largely occurring in the field of plant
breeding and plant genetics itself with the help of plant pathologists.
Plant physiologists and plant biochemists, with a few exceptions,
contributed little to plant breeding practice until 1975.
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DEVELOPMENTS IN PLANT BREEDING AFTER 1975 |
Plant Cell and Tissue Culture
A number of developments in basic plant science started to affect
plant breeding from the early 1970s. The first was the further development of plant cell and tissue culture. The use of embryo rescue
techniques to achieve hybridization with less-related species started
earlier. The introduction of the nematode resistance gene Mi
from wild tomato (Lycopersicon peruvianum) into the
cultivated tomato (Lycopersicon esculentum) on the basis of
an interspecific hybrid obtained by embryo rescue (7) is a very
successful illustration of the usefulness of this technology.
Improvement of cell culture techniques and the possibility to
regenerate plants from a single cell gave the promise of efficient
selection at the cell and tissue culture level, especially for traits
such as stress tolerance. These expectations have not been met because
of several reasons, one of them being that many selected variants
turned out not to be of a genetic nature and also because cells in
culture do not always behave the same as plants in the field. After the
initial surprise that not all plants regenerated from a specific
genotype by tissue culture were identical, plant breeders saw
this phenomenon as another potential source of useful genetic
variation. Larkin and Scowcroft (3) coined the term "somaclonal
variation" for this, which was almost immediately generally accepted.
However, because stable mutations occurring in tissue culture are
mostly negative, as are mutations induced by classical mutagens such as
irradiation and chemicals, this technique did not provide the extra
source of novel and unique genetic variation that some had expected.
Protoplast fusion is another cell and tissue culture technique of which
the first papers describing successful experiments were published in
the 1970s. The tomato-potato hybrid reported by Melchers et al. (4)
was one of the first examples that suggested that this technique could
expand the germplasm pools available for breeders. However, it appeared
that this technique was of limited value because of problems with
somatic incongruity, which did not allow generating hybrids that were
sufficiently fertile for further breeding when the parents are too
distantly related. An intrinsic novelty of somatic hybridization is the
possibility to create novel combinations of organelles such as
chloroplasts and mitochondria, which allowed the successful
introduction of the mitochondrial-encoded male sterility from
Raphanus sativus into Brassica
napus without the unwanted R. sativus
chloroplasts (5). An important application of tissue culture is the
development of haploid induction procedures, either by anther culture
or by chromosome elimination. The latter technique also requires tissue culture technology as well as the in vitro maintenance and rapid propagation of breeding material.
The Cloning of Useful Genes and Transgenic Plants
Until recently only those genes available within the germplasm of
the crop plant and some related species were available for breeding.
However, when transformation procedures were developed that allowed the
introduction of DNA into an organism, almost any gene became available.
Developments in molecular biology allowed the cloning of specific genes
to be used for transformation as well as the control of their
expression. The use of Agrobacterium tumefaciens as a
versatile vector for transformation was an important breakthrough, even
more so in the 1990s when it was convincingly shown that it also could
be used on cereals, which as the seed legumes had been among the
most recalcitrant to transformation. Other technological breakthroughs
were the use of cell- and plant-selectable markers and the development
of novel transformation techniques (1). The latter techniques include
the use of biolistics and simpler techniques for A. tumefaciens-mediated transformation such as explant transformation
and, for Arabidopsis, the extremely efficient and simple floral dip or
vacuum infiltration procedure. Useful genes for plant breeding are
already abundant and could be used to solve previously
impossible or very difficult-to-solve problems. These include
resistance to insects using Bacillus thuringiensis genes, resistance to viruses using coat protein immunization, gene-silencing strategies, and an increase in general resistance by the
introduction of constitutively systemic acquired resistance. In
addition to improving the tolerance and/or resistance to biotic and
abiotic stress, genetic modification offers many possibilities for
modifying the development of plants and their chemical composition. Examples of developmental changes include the engineering of male sterility, the modification of fruit ripening, and alterations in
flowering behavior and plant architecture. The chemical compositions of
fruits and seeds can even be modified so that they can produce non-plant compounds such as antibodies and biodegradable plastics (6).
The possibility to obtain rice varieties with a high level of vitamin A
and a better iron uptake, which could alleviate the nutritional
problems of many people, is very appealing (11). Among the novel traits
introduced with this technology was herbicide resistance, which raised
an emotional aversion against transgenic plants among consumers because
they did not want (more) herbicides to be used. Although it is obvious
that this technology has tremendous possibilities for plant breeding
and human well being, it appears that this is the first time that the
introduction of a novel biological technique became the subject of such
public scrutiny. It is remarkable that similar concerns about
transgenics are virtually absent in the area of medical applications.
Marker-Assisted Breeding
In addition to genetic modification, molecular biology has
provided another tool for plant breeders: DNA markers. This tool seems
to have provoked fewer disputes among the public, probably because it
affects the intrinsic properties of crops less directly. The selection
of superior genotypes is often hampered by the significant influence
that environmental factors have on the expression of a trait and the
variability of these environmental factors. This is especially true for
traits related to crop yield. In addition to their sensitivity to
environment and the phenomenon of genotype-by-environment interaction,
(i.e. the differential reaction of genotypes to environmental changes),
such traits are often controlled by a large number of genes. These
factors make it difficult to analyze their genetic basis and,
therefore, complicate breeding. The efficiency of selection for such
traits can be improved when one can monitor the genotype directly. This
can be done when one knows either the genes responsible for the traits
or genes that are closely linked to them. Many molecular techniques are
now available for monitoring such genes. The application of these
require: (a) the presence of polymorphisms at the DNA level
that can be analyzed easily and cost effectively (often by
using PCR), and (b) knowledge about the genetic location of molecular
markers in relation to the traits of interest. The assessment of the
approximate map position of the genes responsible for the observed
quantitative genetic variation (called quantitative trait loci
[QTL]), can be done by scanning the markers on an ordered linkage map
for association with trait values in a segregating mapping population.
This detailed knowledge of the genetics of complex traits can then be
used to select indirectly for the desired characteristics on the basis
of markers only.
QTL mapping not only enables localization of polygenes on a linkage
map, it also allows the estimation of the effects of individual QTL as
well as their joint effects (epistasis). In a number of studies, this
approach has revealed the environment dependence of QTL effects, thus
helping to elucidate the phenomenon of genotype-by-environment interaction. QTL analysis thus has generated detailed knowledge on the
genetics of complex traits and at the same time provided plant breeders
with a useful tool for indirect selection. The study of QTL at the
molecular level will become increasingly feasible as shown by the
recent cloning of a fruit-size-determining gene (Fig.
1) in tomato (2).
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Figure 1.
Genetic variation among cultivars and related
species of tomato for fruit characteristics which includes variation
for size, shape, and color. Variation is shown both for immature fruit
color ranging from pale to dark green and for mature fruit color
ranging from yellow-green in small-fruited species such as wild tomato
(L. peruvianum) to red and yellow. Domestication of tomato
was accompanied by a dramatic increase in fruit size (compare the small
fruits of the wild species and the large fruits of some of the
cultivars). Frary et al. (2) demonstrated that one of the genes that
controls this quantitative trait could be cloned.
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Another extremely useful application of marker technology is
marker-assisted introgression. The introgression of single genes from
exotic germplasm into breeding material by repeated backcrossing is
greatly facilitated by the use of markers because the donor and the
recipient genome fractions can be monitored in the successive generations of backcrossing. The number of generations required to
recover an improved near-isogenic introgression line can thus be
reduced by 50%, in comparison with the classical procedure. This
"marker-guided introgression" is now being routinely applied in the
breeding programs of several crops.
It is not only monogenic traits that are amenable to "guided
introgression." By combining the QTL approach with backcrossing, useful genes that control quantitative traits have been identified in
the germplasm of plants not adapted to agriculture and have successfully been transferred to advanced breeding lines. The identification of alleles that increase fruit size in the small-fruited wild tomato (Lycopersicon pimpinellifolium) is an appealing
example of this (9). Stuber et al. (8) similarly were able
to create enhanced inbred lines of maize (Zea mays) using
obsolete inbreds as donors, resulting in F1
hybrids that significantly outyielded the original hybrid. Tanksley and
McCouch (10) have expressed the opinion that "unlocking the
genetic potential from the wild" using this approach will be a major
tool for future crop improvement. Molecular analysis has revealed that
the germplasm of wild relatives, either still available in the wild or
conserved in gene banks, is vastly broader than the narrow gene pools
of cultivated plant species.
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THE FUTURE |
The developments described above imply that in plant breeding the
paradigm has changed from selection of phenotypes toward selection of
genes, either directly or indirectly. Plant breeders try to optimize
the use of the genetic variation in nature by bringing together in one
genotype alleles that maximize yield, resistance to stress, etc.
However, because genes do not function as single entities it is
necessary to know how numerous genes function together. This, in turn,
requires knowledge of the potential and constraints of biological
functions of plants. The understanding of the interaction between
genes, organs, and environmental factors, which include other
organisms, is a major challenge for plant biologists. To obtain this
information, it is important to exploit the tools of classical
and molecular genetics. To these disciplines a set of technologies
summarized as "genomics" has recently been added.
Knowledge of the factors that limit the functioning of plants is
essential and may be used to design the ideal plant type. When the
factors that are limiting the optimal functioning of plants are known,
relevant genes can be identified to enable repair of the "defect."
Thereafter, such genes could be searched for in the available
germplasm. To this end, it is important to have access to all existing
genetic variation both within and outside the species. The possibility
to transfer genes across almost all taxonomic borders by molecular
techniques has expanded the potential resources available to plant
breeders enormously. It is becoming generally accepted that a
multidisciplinary approach to plant biology will lead to the
disappearance of borders between disciplines and the irrelevant
difference between classical and modern (molecular) plant breeding.
In the same vein, the differences between transgenic and
non-transgenic crops should become irrelevant when the focus of plant
breeding is on achieving maximal production in a sustainable way to
feed the growing human population.
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FOOTNOTES |
*
Corresponding author; e-mail
maarten.koornneef{at}genetics.dpw.wau.nl; fax
31-317-48-31-46.
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© 2001 American Society of Plant Physiologists
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INTRODUCTION
DEVELOPMENTS IN PLANT BREEDING...
