Abstract
The distribution of transposable elements (TEs) in a genome reflects a balance between insertion rate and selection against new insertions. Understanding the distribution of TEs therefore provides insights into the forces shaping the organization of genomes. Past research has shown that TEs tend to accumulate in genomic regions with low gene density and low recombination rate. However, little is known about the factors modulating insertion rates across the genome and their evolutionary significance. One candidate factor is gene expression, which has been suggested to increase local insertion rate by rendering DNA more accessible. We test this hypothesis by comparing the TE density around germline- and soma-expressed genes in the euchromatin of Drosophila melanogaster. Because only insertions that occur in the germline are transmitted to the next generation, we predicted a higher density of TEs around germline-expressed genes than soma-expressed genes. We show that the rate of TE insertions is greater near germline- than soma-expressed genes. However, this effect is partly offset by stronger selection for genome compactness (against excess noncoding DNA) on germline-expressed genes. We also demonstrate that the local genome organization in clusters of coexpressed genes plays a fundamental role in the genomic distribution of TEs. Our analysis shows that—in addition to recombination rate—the distribution of TEs is shaped by the interaction of gene expression and genome organization. The important role of selection for compactness sheds a new light on the role of TEs in genome evolution. Instead of making genomes grow passively, TEs are controlled by the forces shaping genome compactness, most likely linked to the efficiency of gene expression or its complexity and possibly their interaction with mechanisms of TE silencing.
Highlights
Transposable elements (TEs) are selfish genomic elements on the order of one to several kilobases in length
Along with recombination rate, selection for local genome compactness is the major determinant of local TE density in the fruitfly
The distribution of TEs is affected by randomness in both the location of new insertion and their retention through successive generations in the face of genetic drift, as well as by the idiosyncrasies of individual element families in their modes of transposition and target site preferences
Summary
Transposable elements (TEs) are selfish genomic elements on the order of one to several kilobases in length. Studies on the distribution of TEs in the genomes of D. melanogaster, Caenorhabditis elegans, Arabidopsis thaliana, and humans have shown that elements tend to be enriched in regions of low gene density [5,6,7,8], with the notable exception of human SINE elements [7]. Negative selection is thought to result either from the insertion of TEs into functional regions or from ectopic recombination, events of crossing-over between identical elements at different chromosomal positions, which generate deleterious chromosome rearrangements [15]. Under both mechanisms TE density is predicted to increase with low Editor: Harmit S.
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