Genome organization and gene expression shape the transposable element distribution in the Drosophila melanogaster euchromatin - PubMed (original) (raw)

Genome organization and gene expression shape the transposable element distribution in the Drosophila melanogaster euchromatin

Pierre Fontanillas et al. PLoS Genet. 2007 Nov.

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.

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Conflict of interest statement

Competing interests. The authors have declared that no competing interests exist.

Figures

Figure 1

Figure 1. TE Insertions and Selection for Genome Compactness

(A,B) The correlation between the length of noncoding sequences and the length of TE insertions for genes and intergenic regions. To avoid interaction or facilitation effects in the case of multiple insertions, only unique insertions (by gene or intergenic region) were incorporated in this analysis. (C,D) The nonlinear relationship between the length of noncoding sequences and the proportion of genes or intergenic regions with TE insertion(s). The lines represent the linear model (estimate and standard error) for this correlation (quasibinomial GLM on presence/absence of insertion[s] in genes and intergenic regions).

Figure 2

Figure 2. Number of TE Insertions in Intergenic Regions and Genes as a Function of the Proportion of Germline-Expressed Neighbors

The figure represents the coefficients (±95% confidence intervals) from the GLM analysis presented in Table 1. The number of TE insertions per gene and intergenic region shown on the _y_-axis is corrected for the effect of four covariables entered in the GLM (cf., Table 1): recombination rate, intergenic region or intron + UTR length, proportion of conserved elements, and chromosome (X versus autosomes).

Figure 3

Figure 3. Length of Intergenic Regions and Introns + UTRs as a Function of the Proportion of Germline-Expressed Neighbors

The figure represents the coefficients (±95% confidence intervals) of a log-gaussian GLM analysis of noncoding length of genes/length of intergenic regions as a function of the factors tissue of expression (germline versus soma), element (gene versus intergenic), and neighborhood (proportion of germline-expressed genes among the ten neighbors). The figure illustrates that the effect of the genomic neighborhood depends both on the identity of the genomic element (gene versus intergenic region) as well as the expression type, a fact reflected in the significant triple interaction term in the GLM (F = 4.19, p < 0.05).

Figure 4

Figure 4. Number of TE Insertions for Genes and Intergenic Regions in Transcriptional and Nontranscriptional Territories

This figure is a representation of a GLM analysis including recombination, noncoding length, proportion of conserved sequences, chromosome (X versus autosomes), territory (transcriptional territories versus nontranscriptional territories), tissue of expression (germline versus soma), and element (gene versus intergenic regions) (see Table S6). The triple interaction among the last three factors is significant (F = 8.8, p < 0.01). The figure shows the coefficients and their 95% confidence intervals and the number of intergenic regions and genes, respectively.

Figure 5

Figure 5. Schematic Representation of TE Dynamics in the Euchromatin of D. melanogaster

This figure illustrates the distribution of TEs in and between germline-expressed and soma-expressed genes (in white and black, respectively) within and outside transcriptional territories.

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