Comparative genome analysis of monocots and dicots, toward characterization of angiosperm diversity

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Abstract

The importance of angiosperms to sustaining humanity by providing a wide range of ‘ecosystem services’ warrants increased exploration of their genomic diversity. The nearly completed sequences for two species representing the major angiosperm subclasses, specifically the dicot Arabidopsis thaliana and the monocot Oryza sativa, provide a foundation for comparative analysis across the angiosperms. The angiosperms also exemplify some challenges to be faced as genomics makes new inroads into describing biotic diversity, in particular polyploidy (genome-wide chromatin duplication), and much larger genome sizes than have been studied to date.

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:

  • •

    of special interest

  • ••

    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.

References (72)

  • L Lukens et al.

    Comparison of a Brassica oleracea genetic map with the genome of Arabidopsis thaliana

    Genetics

    (2003)
  • L Meng et al.

    Methylation of the exon/intron region in the Ubi1 promoter complex correlates with transgene silencing in barley

    Plant Mol Biol

    (2003)
  • D Tilman et al.

    Agricultural sustainability and intensive production practices

    Nature

    (2002)
  • Raven P, Evert R, Eichhorn S: Biology of Plants. New York: Worth Publishers, Inc.;...
  • Y.W Yang et al.

    Rates of nucleotide substitution in angiosperm mitochondrial DNA sequences and dates of divergence between Brassica and other angiosperm lineages

    J Mol Evol

    (1999)
  • T.A.G Initiative

    Analysis of the genome sequence of the flowering plant Arabidopsis thaliana

    Nature

    (2000)
  • S.A Goff et al.

    A draft sequence of the rice genome (Oryza sativa L. ssp japonica)

    Science

    (2002)
  • T Sasaki et al.

    The genome sequence and structure of rice chromosome 1

    Nature

    (2002)
  • Q Feng et al.

    Sequence and analysis of rice chromosome 4

    Nature

    (2002)
  • T.R.C.S Consortium

    In-depth view of structure, activity, and evolution of rice chromosome 10

    Science

    (2003)
  • J Yu et al.

    A draft sequence of the rice genome (Oryza sativa L. ssp indica)

    Science

    (2002)
  • G.M Rubin et al.

    Comparative genomics of the eukaryotes

    Science

    (2000)
  • A.L Vettore et al.

    Analysis and functional annotation of an expressed sequence tag collection for tropical crop sugarcane

    Genome Res

    (2003)
  • S Nasu et al.

    Search for and analysis of single nucleotide polymorphisms (SNPs) in rice (Oryza sativa, Oryza rufipogon) and establishment of SNP markers

    DNA Res

    (2002)
  • X Draye et al.

    Toward integration of comparative genetic, physical, diversity, and cytomolecular maps for grasses and grains, using the Sorghum genome as a foundation

    Plant Physiol

    (2001)
  • E Coe et al.

    Access to the maize genome: an integrated physical and genetic map

    Plant Physiol

    (2002)
  • W.W Cai et al.

    An anchored framework BAC map of mouse chromosome 11 assembled using multiplex oligonucleotide hybridization

    Genomics

    (1998)
  • R.G Kynast et al.

    A complete set of maize individual chromosome additions to the oat genome

    Plant Physiol

    (2001)
  • Sorrells ME, La Rota M, Bermudez-Kandianis CE, Greene RA, Kantety R, Munkvold JD, Miftahudin, MA, Ma XF, Gustafson PJ...
  • R.J Mural et al.

    A comparison of whole-genome shotgun-derived mouse chromosome 16 and the human genome

    Science

    (2002)
  • S.F Smith et al.

    Analyses of the extent of shared synteny and conserved gene orders between the genome of Fugu rubripes and human 20q

    Genome Res

    (2002)
  • T.H Lan et al.

    An EST-enriched comparative map of Brassica oleracea and Arabidopsis thaliana

    Genome Res

    (2000)
  • M Rossberg et al.

    Comparative sequence analysis reveals extensive microcolinearity in the Lateral suppressor regions of the tomato, Arabidopsis, and Capsella genomes

    Plant Cell

    (2001)
  • B Stirling et al.

    Comparative sequence analysis between orthologous regions of the Arabidopsis and Populus genomes reveals substantial synteny and microcollinearity

    Canadian Journal of Forest Research

    (2003)
  • H Liu et al.

    Comparative genomics between rice and Arabidopsis shows scant collinearity in gene order

    Genome Res

    (2001)
  • K.M Devos et al.

    Arabidopsis — rice: will colinearity allow gene prediction across the eudicot-monocot divide?

    Genome Res

    (1999)
  • Mayer K, Murphy G, Tarchini R, Wanbutt R, Volckaert G, Pohl T, Dusterhoft, Andreas, Stiekema W, Entian K-D, Terryn N,...
  • H.M Ku et al.

    Comparing sequenced segments of the tomato and Arabidopsis genomes: large-scale duplication followed by selective gene loss creates a network of synteny

    Proc Natl Acad Sci USA

    (2000)
  • D Grant et al.

    Genome organization in dicots: genome duplication in Arabidopsis and synteny between soybean and Arabidopsis

    Proc Natl Acad Sci USA

    (2000)
  • M Lee et al.

    Expanding the genetic map of maize with the intermated B73 × Mo17 (IBM) population

    Plant Mol Biol

    (2002)
  • H.H Yan et al.

    Estimates of conserved microsynteny among the genomes of Glycine max

    Theor Appl Genet

    (2003)
  • H.Y Zhu et al.

    Syntenic relationships between Medicago truncatula and Arabidopsis reveal extensive divergence of genome organization

    Plant Physiol

    (2003)
  • G Stebbins

    Chromosomal variation and evolution; polyploidy and chromosome size and number shed light on evolutionary processes in higher plants

    Science

    (1966)
  • J Masterson

    Stomatal size in fossil plants — evidence for polyploidy in majority of angiosperms

    Science

    (1994)
  • J.M McGrath et al.

    Duplicate sequences with a similarity to expressed genes in the genome of Arabidopsis thaliana

    Theor Appl Genet

    (1993)
  • S.P Kowalski et al.

    Comparative mapping of Arabidopsis thaliana and Brassica oleracea chromosomes reveals islands of conserved organization

    Genetics

    (1994)

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