Transposon Occupation in Eukaryotic Genomes

Transposable elements, or transposons, are selfish genetic elements that possess the ability to mobilize within a genome, potentially causing serious damage. They can accomplish this through several well-understood mechanisms. Most move via an RNA intermediate (class I: retrotransposons), whereas others colonize new locations through the direct transfer of transposon DNA (class II: DNA transposons) (for review, see Slotkin and Martienssen 2007). In the case of retrotransposons, ac tive elements within the genome are transcribed and translated into functional proteins that subsequently generate an additional DNA copy of the element and catalyze its integration into a new genomic site. DNA transposons are also transcribed and translated into proteins that instead excise a physical DNA copy of an element from the genome and then insert that DNA elsewhere in the genome. This “cut-and-paste” mechanism generates no net increase in copies of the element on an individual level (although small genomic lesions are left behind), whereas retrotransposition actively increases transposon copy number within an individual genome. In both cases, transposon mobilization can have positive and negative consequences for the viability of an organism and its progeny, notably on the organization of its genome. The potential detrimental effects of unregulated transposon activity are obvious. For example, by inserting into an essential gene, especially one with a sensitive dosage requirement, a transposon could severely alter cell or organismal viability. The impact of landing in a nonessential gene is less dramatic, but such events can still generate clear phenotypic manifestations (Demerec 1926a,b). Transposition into important gene regulatory regions, such as splicing regulators or transcriptional enhancer domains, could significantly change transcriptional and posttranscriptional gene expression programs (White et al. 1994). Moreover, transposons can promote alterations in chromosomal structure by generating double-stranded DNA breaks that can precede the formation of unstable dicentric and acentric chromosomes (McClintock 1950) and induce other spurious chromosomal aberrations. Finally, important chromatin domains, such as insulator and boundary elements, can be interrupted, leading to a general transcriptional misregulation in the surrounding genomic space. Not all instances of transposon mobilization necessarily lead to such negative consequences for an organism. In fact, transposons are capable of positively influencing genomic content, structure, and evolution (Kazazian 2004). For instance, transposon movement can lead to the gain or loss of introns and exons, generating novel transcriptional output. They can also generate additional coding information in the genome, either being themselves domesticated as components of host transcripts (Miller et al. 1992; Baudry et al. 2009) or by inducing duplication of endogenous genes (Esnault et al. 2000). Transposon-induced reorganization of large chromosomal tracts can drive substantial genome-scale evolution, assuming creation of a positive selective advantage. Likewise, reorganization of transcriptional regulatory regions can drive the evolution of expression programs through either disruption or donation of novel regulatory elements. Finally, transposon-induced chromatin state changes can modify the genomic landscape by producing new broadscale regulatory domains, perhaps creating variation by altering the transcriptional output at particular developmental stages. Each of these types of events can provide substrates for evolutionary selection and thus have profound impacts on the adaptability of the organism. Molecular Evolution of piRNA and Transposon Control Pathways in Drosophila