Genome Size Reduction through Illegitimate Recombination Counteracts Genome Expansion in <em>Arabidopsis</em>
Abstract
Genome size varies greatly across angiosperms. It is well documented that, in addition to polyploidization, retrotransposon amplification has been a major cause of genome expansion. The lack of evidence for counterbalancing mechanisms that curtail unlimited genome growth has made many of us wonder whether angiosperms have a “one-way ticket to genomic obesity.” We have therefore investigated an angiosperm with a well-characterized and notably small genome, Arabidopsis thaliana, for evidence of genomic DNA loss. Our results indicate that illegitimate recombination is the driving force behind genome size decrease in Arabidopsis, removing at least fivefold more DNA than unequal homologous recombination. The presence of highly degraded retroelements also suggests that retrotransposon amplification has not been confined to the last 4 million years, as is indicated by the dating of intact retroelements.
Flowering plants (angiosperms) vary enormously in genome size, from <50 Mb in some members of the Cruciferae to >85,000 Mb in some Liliaceae (Bennett and Leitch 1995). The mechanisms that account for dramatic expansion of angiosperm genomes have been documented, primarily polyploidization and retrotransposon amplification (SanMiguel et al. 1996, 1998; Wendel 2000); however, counterbalancing modes of genome contraction have not been convincingly shown. In the absence of an equally comprehensive and aggressive mechanism for genome size decrease, the question remains whether angiosperms have a “one-way ticket to genome obesity” (Bennetzen and Kellogg 1997). We have addressed this fundamental issue in the genome size debate by studying the structure and evolution of long terminal repeat (LTR) retrotransposons in Arabidopsis.
LTR retrotransposons constitute a large part of the repetitive DNA fraction in plant species. They are characterized by LTRs that vary in size from a few 100 base pairs (bp) to several kilobases and terminate in short inverted repeats, usually 5′-TG-3′ and 5′-CA-3′ (Kumar and Bennetzen 1999). The well-defined structure of LTR retrotransposons, their prevalence and dispersion in the genome, their acknowledged role in genome size expansion, and the fact that individual elements have little or no selective significance make LTR retrotransposons suitable elements for studying genome evolution (Petrov 2001). The prevalence and distribution of LTR retrotransposons have been the subject of several studies, including in Arabidopsis (Marín and Lloréns 2000; Terol et al. 2001). These studies, however, are generally based on the analysis of intact elements of relatively recent origin and provide no information on the long-term fate of these sequences. In our study, LTR-retrotransposon families were established on the basis of homology of the LTRs rather than the open reading frames. An important advantage of this approach is that not only complete elements but also solo LTRs and elements that have undergone a variety of deletions can be identified. It is precisely the structure of this latter group that provides the most important clues regarding plant genome evolution.
LTR, long terminal repeat; PBS, primer-binding site; PPT, polypurine tract; DR, direct repeat.
Acknowledgments
K.M. Devos acknowledges funding from the Biotechnology and Biological Sciences Research Council (BBSRC) through a David Phillips Research Fellowship and ISIS International Fellowship, and J.L. Bennetzen thanks NSF for supporting this research (Grant 9975793).
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Footnotes
E-MAIL ku.ca.crsbb@soved.neirtaK; FAX 44 1603 450 023/24.
Article and publication are at http://www.genome.org/cgi/doi/10.1101/gr.132102.