"What You Need, Baby, I Got It": Transposable Elements as Suppliers of Cis-Operating Sequences in Drosophila

Abstract

Transposable elements (TEs) are constitutive components of both eukaryotic and prokaryotic genomes. The role of TEs in the evolution of genes and genomes has been widely assessed over the past years in a variety of model and non-model organisms. Drosophila is undoubtedly among the most powerful model organisms used for the purpose of studying the role of transposons and their effects on the stability and evolution of genes and genomes. Besides their most intuitive role as insertional mutagens, TEs can modify the transcriptional pattern of host genes by juxtaposing new cis-regulatory sequences. A key element of TE biology is that they carry transcriptional control elements that fine-tune the transcription of their own genes, but that can also perturb the transcriptional activity of neighboring host genes. From this perspective, the transposition-mediated modulation of gene expression is an important issue for the short-term adaptation of physiological functions to the environmental changes, and for long-term evolutionary changes. Here, we review the current literature concerning the regulatory and structural elements operating in cis provided by TEs in Drosophila. Furthermore, we highlight that, besides their influence on both TEs and host genes expression, they can affect the chromatin structure and epigenetic status as well as both the chromosome's structure and stability. It emerges that Drosophila is a good model organism to study the effect of TE-linked regulatory sequences, and it could help future studies on TE-host interactions in any complex eukaryotic genome.

Keywords: Drosophila melanogaster; cis-regulatory elements; enhancer; genome evolution; heterochromatin; insulator; promoter; transposable elements.

Figure 1

(A) Structural features of the TEs identified and described in Drosophila. The symbols used are described on the left part of the panel. (B) Overview of the number of TE families belonging to each of the main groups of TEs in D. melanogaster and in other Drosophila species (source: http://flybase.org, last access December 2019).

Figure 2

Schematic representation of the key effects produced by the cis-operating sequences upon TE insertion. Symbols are explained in the box.

Figure 3

In situ hybridization performed on wild type (panels A and B) or mutant (panel C) ovaries using GS1 (panel A) or Tirant (panels B and C) specific probes. The organization of the relevant locus in the 21B region of the polytene chromosomes of D. melanogaster is provided.