What transposable elements tell us about genome organization and evolution: the case of <i>Drosophila</i>

Abstract

Transposable elements (TEs) have been identified in every organism in which they have been looked for. The sequencing of large genomes, such as the human genome and those of Drosophila, Arabidopsis, Caenorhabditis, has also shown that they are a major constituent of these genomes, accounting for 15% of the genome of Drosophila, 45% of the human genome, and more than 70% in some plants and amphibians. Compared with the 1% of genomic DNA dedicated to protein-coding sequences in the human genome, this has prompted various researchers to suggest that the TEs and the other repetitive sequences that constitute the so-called “noncoding DNA”, are where the most stimulating discoveries will be made in the future (Bromham, 2002). We are therefore getting further and further from the original idea that this DNA was simply “junk DNA”, that owed its presence in the genome entirely to its capacity for selfish transposition. Our understanding of the structures of TEs, their distribution along the genomes, their sequence and insertion polymorphisms within genomes, and within and between populations and species, their impact on genes and on the regulatory mechanisms of genetic expression, their effects on exon shuffling and other phenomena that reshape the genome, and their impact on genome size has increased dramatically in recent years. This leads to a more general picture of the impact of TEs on genomes, though many copies are still mainly selfish or junk DNA. In this review we focus mainly on discoveries made in Drosophila, but we also use information about other genomes when this helps to elucidate the general processes involved in the organization, plasticity, and evolution of genomes.

The shrunken genome of Arabidopsis thaliana

“…Furthermore, polyploidy is known to occur at the tips of the Brassicaceae tree, for example in the genera Arabidopsis and Boechera (Clauss and Koch 2006;Schranz et al 2005). Meanwhile, the importance of transposable elements in genome evolution is also well documented (Bartolome et al 2002;Bennetzen 2000;Biemont and Vieira 2005;Kumar and Bennetzen 1999;Lenoir et al 2005). Thus, it is not surprising that our sequenced clones revealed a correlation between the presence of transposable elements and increases in the size of homologous regions (see online supplementary data associated with this article).…”

Population dynamics of PIWI-interacting RNAs (piRNAs) and their targets in Drosophila

“…Due to their high copy number, TEs have had profound effects on the structure, content, and evolution of genomes (Biemont et al 1999;Kidwell and Holyoake 2001;Kazazian 2004;Ashburner and Bergman 2005;Biemont and Vieira 2005;Bergman et al 2006). TEs can mediate evolution of genome structures through their tendency to nucleate chromosomal rearrangements (Hoogland and Biemont 1996;Petrov et al 2003;Biemont and Vieira 2006), their contribution to the creation of new genes (Britten 2006;Kaessmann et al 2009), and their de novo generation of new regulatory motifs for neighboring genes (Lowe et al 2007).…”

Genome size evolution: Within-species variation in genome size

“…In addition to the impact of the effective population size (Lynch and Conery, 2003), at least two explanations are conceivable. A global change could have occurred as a result of the stressful environmental conditions encountered by the species when they invaded new geographical areas, or of confrontations between populations that had not encountered each other earlier (Biémont and Vieira, 2005 and references therein). TE transposition and amplification have been reported in inter-species hybrids in Drosophila and in the Australian wallaby (see references in Biémont and Vieira, 2005), but few data are available about intra-species hybridization.…”

“…A global change could have occurred as a result of the stressful environmental conditions encountered by the species when they invaded new geographical areas, or of confrontations between populations that had not encountered each other earlier (Biémont and Vieira, 2005 and references therein). TE transposition and amplification have been reported in inter-species hybrids in Drosophila and in the Australian wallaby (see references in Biémont and Vieira, 2005), but few data are available about intra-species hybridization. Only certain specific TEs, as in dysgenic crosses in Drosophila (Kidwell, 2002), or other kinds of repeated sequence, may be involved.…”