Comparative genome analysis of monocots and dicots, toward characterization of angiosperm diversity
Introduction
The angiosperms, or flowering plants, provide ecosystem services including oxygen, fuel, medicines, erosion and flood control, soil regeneration, and other benefits [1] that are absolutely essential to humanity and indeed are a cornerstone of the global ecosystem. The ‘domestication’ of about 200 angiosperms to provide most of the world’s supply of food, feed and fibre has largely determined our ability to sustain modern human populations and has also empowered human social development [2]. A small subset of domesticates, plus a few botanical models such as Arabidopsis thaliana, account for most of our present knowledge of the repertoire, organization and function of plant genes.
The past two decades of plant molecular genetics research, and in particular the past few years of high-throughput genomics, have set the stage for new advances in comparative biology. For the first time, we have access to large numbers (and in some cases all) of the genes in a genome, albeit for a small subset of angiosperms. Now we can begin the long process of sifting through the many molecular-level differences that have accumulated during the approximately 170–235 million years [3] since the angiosperms diverged from a common ancestor, to seek specific changes that contribute to variation in life history traits, biochemistry, morphology and development, and adaptation to the biotic and abiotic environment.
While comparative biology offers valuable insight into divergence at many taxonomic levels, of particular interest is comparison of members of the two major angiosperm subclasses, monocots and dicots. The largely finished sequence of the dicot Arabidopsis [4], together with the rapidly progressing sequence of the monocot Oryza (rice) 5.••, 6.••, 7.••, 8.••, 9.•• provide a natural framework for this work. Genetic maps, physical maps and expressed sequence tag (EST) resources for a host of additional taxa permit early assessments of diversity within each of the angiosperm subclasses, and provide important contextual information by which to better relate major events in the Arabidopsis and Oryza lineages to the plant family tree. In this review, we explore early messages arising from comparison of the content and organization of monocot and dicot genomes, address key consequences of polyploidy for angiosperm comparative genomics, and compare and contrast methods that are likely to be important to further description and study of angiosperm genomic diversity.
Section snippets
Gene repertoire
Many functions in diverse eukaryotes are directed by genes that exhibit much similarity at the amino acid and even nucleotide level [10], including the angiosperms. The Arabidopsis transcriptome is currently estimated to include 30 078 genes (http://www.ncbi.nlm.nih.gov). The rice transcriptome appears to be more complex, with estimates based on genomic shotgun sequencing of 46 022–55 615 genes [9••] and 32 277–61 668 genes [5••]. Higher estimates based on finished sequencing (62 500 genes [6••]
Chromosome and genome organization
Given that the vast majority of angiosperms lack complete sequences, genetic maps continue to be a central tool for studying their chromosome organization. Most major crops, and many botanical models, enjoy detailed sequence-tagged site (STS)-based genetic recombination maps that are suitable not only for comparative biology, but also for crop improvement. While these maps have been successfully applied to many needs using traditional restriction-fragment length polymorphism or simple sequence
Ancient polyploidy and its consequences
Comparative studies of plant chromosome evolution show important differences from early results in animals. Gene order conservation along the chromosomes of vertebrates is evident after hundreds of millions of years of divergence 18., 19., but comparisons of the Arabidopsis sequence to partial gene orders of other angiosperms (flowering plants) sharing common ancestry ∼170–235 million years ago [3] have yielded conflicting results. Although gene order conservation is considerable in confamilial
Further insights into angiosperm genomic diversity
While botanical models provide seminal information that can be extrapolated to a degree by comparative approaches, comprehensive information about angiosperm diversity will require detailed exploration of many additional genomes. The greatest challenge to their widespread genomic analysis, and a practical motivation for many comparative genomics efforts, is that angiosperms exhibit about 1000-fold variation in genome size due mostly to repetitive DNA. EST sequencing is a first step toward
Conclusions
The identification of multiple polyploidization events in the Arabidopsis lineage, together with methods to mitigate the effects of these events on comparative genomics, sets the stage for a re-evalation of gene order conservation across diverse angiosperms. The Oryza sequence will provide the information needed to study the course of monocot genome evolution, and then to perform truly orthologous comparisons within and among monocots and dicots. Detailed study of these two lineages will
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
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of special interest
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of outstanding interest
Acknowledgements
We thank many members of the Paterson laboratory and our collaborators and colleagues for fruitful discussions. We also thank the US National Science Foundation, US Department of Agriculture, International Consortium for Sugarcane Biotechnology and Georgia Agricultural Experiment Station for financial support.
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