American Journal of Botany 91 10 1709 1725 2004 THE EVOLUTION OF NUCLEAR GENOME STRUCTURE IN SEED PLANTS1 ELIZABETH A KELLOGG2 4 AND JEFFREY L BENNETZEN3 Department of Biology University of Missouri St Louis One University Boulevard St Louis Missouri 63121 USA and 3 Department of Genetics University of Georgia Athens Georgia 30622 USA 2 Plant nuclear genomes exhibit extensive structural variation in size chromosome number number and arrangement of genes and number of genome copies per nucleus This variation is the outcome of a set of highly active processes including gene duplication and deletion chromosomal duplication followed by gene loss amplification of retrotransposons separating genes and genome rearrangement the latter often following hybridization and or polyploidy While these changes occur continuously it is not surprising that some of them should be fixed evolutionarily and come to mark major clades Large scale duplications pre date the radiation of Brassicaceae and Poaceae and correlate with the origin of many smaller clades as well Nuclear genomes are largely colinear among closely related species but more rearrangements are observed with increasing phylogenetic distance however the correlation between amount of rearrangement and time since divergence is not perfect By changing patterns of gene expression and triggering genome rearrangements novel combinations of genomes hybrids may be a driving force in evolution Key words duplication polyploidy retrotransposon Plant nuclear genomes are enormously variable Chromosome number the degree of gene clustering and chromosome size can all differ by as much as an order of magnitude even between closely related species Some variation is generated so rapidly that two different allelic versions of a chromosomal segment otherwise known as haplotypes can be dissimilar in gene content and arrangement even within a single plant species like maize Fu and Dooner 2002 Hence plant nuclear genomes vary sufficiently to serve as powerful differentiating factors Some changes clearly mark particular lineages of seed plants such as the large inversions and translocations that are found within some clades of grasses Gale and Devos 1998 Other changes such as polyploidy and most gene duplications deletions are so frequent that they occur independently in multiple lineages Recent studies have begun to characterize the natures rates and mechanisms of these various types of chromosomal rearrangement thereby providing our first detailed insights into how these changes contribute to current evolved states and how they may be used in phylogenetic analysis This article will describe the standard structural patterns in the nuclear genomes of seed plants and show how these have been conserved over the last 100 million years of angiosperm evolution The natures mechanisms and frequencies of specific chromosomal rearrangements will be described Genome size variation and genome duplication will be discussed in some detail Through this presentation we hope to provide a comprehensive view of the current understanding of plant nuclear genome structure and evolution and indicate future directions of this field of study Much of this review will focus on grasses Poaceae primarily because so much comparative genome structure information is available within this family Comparative sequence analysis has been undertaken in orManuscript received 8 January 2004 revision accepted 15 June 2004 The authors thank the editors of this special issue for inviting them to contribute this article We also thank Simon Malcomber for help with the illustrations and Jonathan Wendel Loren Rieseberg and Associate Editors Jeff Palmer and Mark Chase for comments that greatly improved the manuscript 4 E mail tkellogg umsl edu 1 thologous regions of the barley maize rice sorghum and wheat genomes reviewed in Bennetzen and Ramakrishna 2002 thereby providing a large data set for the characterization of local genome evolution Comparative recombinational maps have also been generated for these species as well as for pearl millet sugarcane foxtail millet rye and a few others Gale and Devos 1998 Hence sufficient data are available only in the grasses for the comprehensive characterization of plant nuclear genome structure and evolution Comparative data are rapidly accumulating for other families however notably for Brassicaceae and we expect that the next several years will see a tremendous increase in information on how genomes evolve Many other important aspects of nuclear genome evolution will not be covered here although fascinating new data are accumulating For example the overall base composition of genomes varies and affects codon usage patterns Codon usage patterns and percentage GC in onion are more similar to Arabidopsis than to rice suggesting although hardly proving that the high GC content of the grasses may be derived Kuhl et al 2004 Intron size and number vary among plants but the correlates of this variation are not well known In animals small genome size correlates with smaller introns but this relationship does not seem to hold in plants see for example Dubcovsky et al 2001 Wendel et al 2002 Base composition rates of substitution and size and number of introns are all important aspects of genome evolution and we hope that more data and analyses will be forthcoming on all topics in the next few years STRUCTURE OF SEED PLANT GENOMES Gross genome structure All angiosperms contain relatively complex nuclear genomes with genes scattered across multiple chromosomes Other plants are less well characterized but their large genome sizes see Bennett and Leitch 2003 for a comprehensive presentation of plant genome sizes indicate that most nonflowering plant genomes are equally complex In even the smallest genomes like Arabidopsis about 140 Mb more than 20 of the DNA is composed of various repetitive elements Arabidopsis Genome Initiative 2000 1709 1710 AMERICAN JOURNAL These repeats include transposable elements and various types of simple tandem repeats including satellite DNA and simple sequence repeats SSRs In most angiosperms transposable elements especially long terminal repeat LTR retrotransposons comprise the vast majority of this repetitive DNA reviewed in Bennetzen 2002a Chromosome numbers are highly variable in the flowering plants and do not generally relate to overall genome size For instance the 440 Mb haploid rice genome is distributed across 12 chromosomes whereas the
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