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Plant Physiol, January 2001, Vol. 125, pp. 152-155
Genomics and Synteny
Susan R.
McCouch*
Plant Breeding Department, 418 Bradfield Hall, Cornell University,
Ithaca, New York 14853-1901
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INTRODUCTION |
Building on early observations about
natural plant variation in time and space, early geneticists, including
Darwin, Mendel, and Vavilov, posed fundamental questions about the
origin, structure, and evolution of genetic diversity. They postulated
that an underlying reservoir of innate and heritable genetic
possibilities delineated the options for the growth, development, and
reproduction of organisms at both the individual and population levels.
The field of plant genetics today continues to address many of the same
questions while integrating developments in molecular and computational biology. Over the last 15 to 20 years, new, highly automated tools have
created unprecedented opportunities for generating and analyzing large
biological data sets, and the systematic processing of nucleic acid and
protein sequence information from many different organisms has
fundamentally changed the way that biologists approach the study of
living things.
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GENOMICS |
The term genome (derived from the words genes and chromosomes) was
first used by Winkler (30) to signify the complete set of chromosomes
and their genes. The term genomics was first used in 1986 to describe
the enterprise that aimed to map and sequence the human genome (18).
The field of genomics takes advantage of the common biological language
represented by DNA and RNA and uses high throughput sequencing
strategies, microchip arrays, digital technology, and computationally
intensive analysis to understand the structure, function, and evolution
of diverse organisms. Applications of genomic technologies in all areas
of biology have lowered the barriers that once separated the plant,
animal, and microbial research communities.
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LINKAGE MAPPING |
The use of restriction fragment length polymorphisms (RFLPs) as
genetic markers made it possible to map, for the first time, an almost
unlimited number of randomly distributed polymorphic loci in a single
population and provided the foundation for efficient, whole-genome
studies at the molecular level. The application of RFLP technology for
genetic mapping was pioneered in humans by Botstein et al. (8). The
distributed nature of restriction enzyme sites and the neutral nature
of restriction enzyme polymorphism turned out to be equally applicable
for genetic map construction in plants. This was first demonstrated by
Bernatzky and Tanksley (4) and Helentjaris et al. (12), whose work
established the foundation for molecular mapping in a wide variety of
plant species over the next decade.
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QUANTITATIVE TRAIT LOCUS (QTL) ANALYSIS |
The advances in molecular linkage mapping unleashed a series of
powerful new methodologies for studying genotype-phenotype relationships. Given the emphasis on diversity (rather than on a single
species) in the plant kingdom, low- or medium-resolution molecular maps
were constructed for numerous plant species over the last 15 years. One
of the rationales for constructing these maps was to facilitate genetic
analysis and characterization of genes underlying both simply and
quantitatively inherited traits. The plant science community was quick
to take advantage of the fecundity, versatility of mating habit (both
inbreeding and outcrossing are possible in most plant species), and
ability to manipulate the reproductive cycle of plant populations to
pioneer QTL analysis using molecular markers (for review, see 26). The
first use of a complete RFLP map for this purpose was reported by
Paterson et al. (22) in tomato (Lycopersicon
sp.), and this study launched an epoch of accelerated mapping
and QTL analysis in plants.
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GENOME DUPLICATION |
At the same time RFLP maps were being used to identify the
position of genes and QTLs along the chromosomes of higher plants, these same maps were defining internally duplicated chromosome segments
within plant genomes. The location and extent of internal duplications
were first documented in the maize (Zea mays) genome (13),
supporting earlier hypotheses describing modern, diploid maize as an
ancient polyploid. More recently, studies of the Brassicaceae family,
of which Arabidopsis is a member, have emphasized the themes of genome
duplication and rearrangement (for review, see 6, 17). Polyploid
ancestry in all biological kingdoms is probably more universal than
once was believed, as postulated by Ohno (20) and demonstrated in yeast
(Saccharomyces cerevisiae; 31). As increasing resolution is achieved in genetic, physical, and sequence-based mapping
studies, detection of genome-wide and fine-scaled duplication is
providing new insights regarding the timing of duplication events and
the types of selection pressures affecting specific genes and/or
genomic regions of plant, animal, and microbial genomes over the course
of evolution.
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COMPARATIVE MAPPING AND HOMEOLOGY-BASED GENE
ISOLATION |
The term synteny (from the Greek; syn = together, taenia = ribbon) is used in genetics to indicate the presence of two or more
loci on the same chromosome. The original relevance of the term dates
to a pregenomics era when locating genes to chromosomes was
accomplished without the advantage of whole-genome mapping technologies. Today, the concept of synteny has been expanded to
address questions of homeology (residual homology of originally completely homologous chromosomes). The earliest whole-genome comparative maps for plants were developed among species in the Solanaceae family. Bonierbale et al. (7) demonstrated that cDNA markers
along the 12 chromosomes of tomato and potato (Solanum tuberosum) were largely collinear, differing only by five
detectable paracentric inversions, whereas pepper (Capsicum
sp.) appears to have a greater propensity for rearrangement.
Studies in the Gramineae family are perhaps the most developed. Common
sets of low-copy cDNA "anchor probes" were used to develop
comparative maps among seven or more different grass family members
(27; for review by Devos and Gale, see 9) and regions of conserved gene order with corresponding positional conservation of phenotypes, attributed to mutants and QTLs, have been well documented (for references, see 23). However, numerous exceptions where linked markers
do not map to the predicted locations within collinear regions have
also been reported (3, 21, 29) and raise interesting questions about
the predictive nature of comparative maps at both low and high levels
of resolution. Kilian et al. (14) were the first to attempt to clone a
gene in one plant species based on detailed positional and sequence
information (i.e. on microsynteny, as it is now called) in a
homeologous region of another genus. Although the corresponding
chromosome segments of barley (Hordeum vulgare) and rice
(Oryza sativa) were clearly homeologous in the region
of the barley stem rust resistance gene Rpg1, the target gene could not be identified in the predicted location in rice. This
study illustrated some of the difficulties associated with the
application of comparative maps to gene isolation efforts, and is also
consistent with evidence suggesting that plant resistance genes may
evolve more rapidly than other kinds of genes (19). Studies of gene
collinearity across ever more divergent genomes have moved from
hybridization-based Southern analysis of cDNA clones (within families)
to more highly automated forms of sequence-based analysis based on
comparisons with model genomes. In a recent study by Ku et al. (16),
microcollinearity between tomato and Arabidopsis was evaluated en route
to identifying a candidate gene for the ovate mutant
controlling fruit shape in tomato. A 105-kb region of the tomato genome
was sequenced and compared with the almost-completed genomic sequence
of Arabidopsis. Rather than a pattern of one-to-one collinearity in a
defined homeologous region, they described distributed networks of
synteny that reflect the various genome duplication events that have
marked the evolution of Arabidopsis since divergence from its last
common ancestor with tomato. The extent of monocot-dicot homeology has
also been addressed, but conclusive evidence on this question awaits
analysis of the emerging genomic sequences of rice and Arabidopsis.
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SEQUENCES AND SEQUENCE DATABASES |
Today, the search for a gene of interest often starts with
sequence information, including expressed sequence tags (ESTs), genomic
sequence, and protein sequence. A major step in making sequence
information publicly available for large-scale analysis was the
formation of GenBank and its counterpart, the European Molecular
Biology Laboratory data library, in 1982 (5). As more and more data is
deposited, these and other databases have become increasingly useful
because there is an ever greater chance of finding sequence similarity
(and inferring potential homology) to a newly sequenced gene. Key to
making sequence information useful to biologists has been the
development of rigorous and efficient algorithms for searching large
databases and distinguishing biologically significant relationships
from chance similarities (2, 24, 25). The value of cDNA sequencing was
first summarized by Adams et al. (1) where they argued that EST
sequencing would be the most efficient and cost-effective way of
tagging most of the genes in an organism long before complete genomic
sequence was available. This approach had the additional appeal of
focusing only on the most conserved portions of diverse genomes and on sequences that were likely to be of functional significance. Full genomic sequencing of even the most compact plant genome(s) represents a major commitment of time and resources, but in contrast with EST
sequencing, is designed to reveal all the genes in an organism. In
addition, genomic sequencing provides information about global genome structure and organization, regulatory regions, transposable elements, and non-coding sequences. Thus, the availability of fully
assembled and annotated genomic sequence for divergent model plant
species, such as Arabidopsis and rice, in addition to many thousands of
ESTs, bacterial artificial chromosome ends, and genomic sequences in multiple other species, helps drive genomics research in
the plant biology community today.
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FUNCTIONAL GENOMICS |
Genetics is the study of variation and inevitably involves a quest
to understand the relationship between genotype and phenotype. For many
years, genetic studies were initiated based on observations of either
naturally occurring or consciously derived phenotypic mutations in an
organism. Insertional mutagenesis, which may involve activation of
native transposons or the introduction of foreign transposons or T-DNA
elements into a genome via plant transformation, provides a way of
knocking out, reducing, enhancing, or completely altering the
expression patterns of specific genes (for review, see 15, 28). The
systematic application of insertional mutagenesis techniques in a
genomics context aims to interrupt or alter the expression of every
gene in an organism as the basis for studying the relationship between
phenotype and genotype. The efficiency of this approach ultimately
depends on the ability to recognize altered phenotypes and rapidly
associate phenotypic changes with specific sequence alternations (i.e.
to identify functional nucleotide polymorphisms). With the availability
of well-saturated genetic and comparative maps, abundant EST and
genomic sequence information, and an increasingly sophisticated set of
computational tools, these populations are increasingly useful as
sources of novel genetic variation and as a tool for studying
structure-function relationships across diverse organisms. Today,
efforts to understand the functional significance of a gene or suite of
genes in virtually any biological context involve both keen observation
of phenotype and intensive computational comparisons of the structural
properties of DNA or protein. Linear approaches to sequence alignment
are increasingly complemented by assessing the more highly conserved, three-dimensional structure of a gene's protein product. In a recent
paper by Frary et al. (10), a major QTL determining fruit size in
tomato was positionally cloned, and in an effort to understand the
gene's function, the predicted structure of the protein product was
compared with others in a protein structure database. The tomato
protein revealed a three-dimensional structure with remarkable similarity to a human oncogene RAS (rat sarcoma, named because it was
first discovered in rat) protein, known to deregulate cell division in humans. This work presents the tantalizing hypothesis that
a common, ancient gene family, whose identity predates the divergence
of plants and animals, may be responsible for controlling fruit size in
tomatoes and tumor development in humans. In a similar vein, work in
plant disease resistance strongly suggests that the defense system in
plants has evolutionary origins in common with the immune system in
mammals (for review, see 11). The ability to recognize these
similarities and to comprehend the logic that supports the arguments
lies at the root of biologists' intrigue with studies of genomics and
synteny today.
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ACKNOWLEDGMENTS |
I gratefully acknowledge help from my graduate students, Michael
Thomson and Jeremy Edwards, during the preparation of this manuscript.
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FOOTNOTES |
*
E-mail srm4{at}cornell.edu; fax 607-255-6683.
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TOP
INTRODUCTION
GENOMICS