Genome canalization: the coevolution of transposable and interspersed repetitive elements with single copy DNA

Abstract

Transposable and interspersed repetitive elements (TIREs) are ubiquitous features of both prokaryotic and eukaryotic genomes. However, controversy has arisen as to whether these sequences represent useless 'selfish' DNA elements, with no cellular function, as opposed to useful genetic units. In this review, we selected two insect species, the Dipteran Drosophila and the Lepidopteran Bombyx mori (the silkmoth), in an attempt to resolve this debate. These two species were selected on the basis of the special interest that our laboratory has had over the years in Bombyx with its well known molecular and developmental biology, and the wealth of genetic data that exist for Drosophila. In addition, these two species represent contrasting repetitive element types and patterns of distribution. On one hand, Bombyx exhibits the short interspersion pattern in which Alu-like TIREs predominate while Drosophila possesses the long interspersion pattern in which retroviral-like TIREs are prevalent. In Bombyx, the main TIRE family is Bm-1 while the Drosophila group contains predominantly copia-like elements, non-LTR retroposons, bacterial-type retroposons and fold-back transposable elements sequences. Our analysis of the information revealed highly non-random patterns of both TIRE biology and evolution, more indicative of these sequences acting as genomic symbionts under cellular regulation rather than useless or selfish junk DNA. In addition, we extended our analysis of potential TIRE functionality to what is known from other eukaryotic systems. From this study, it became apparent that these DNA elements may have originated as innocuous or selfish sequences and then adopted functions. The mechanism for this conversion from non-functionality to specific roles is a process of coevolution between the repetitive element and other cellular DNA often times in close physical proximity. The resulting interdependence between repetitive elements and other cellular sequences restrict the number of evolutionarily successful mutational changes for a given function or cistron. This mutual limitation is what we call genome canalization. Well documented examples are discussed to support this hypothesis and a mechanistic model is presented for how such genomic canalization can occur. Also proposed are empirical studies which would support or invalidate aspects of this hypothesis.

A role for Drosophila in understanding drug-induced cytotoxicity and teratogenesis

“…This is not surprising however, when considering the difference in genome organization of mammals and Drosophila (von Sternberg et al 1992). The Drosophila genome is quite compact as exemplified by the 1 kb Dhfr gene with a lone 50 bp intron and a single TATA sequence for transcription initiation (Hao et al 1994).…”

Three novel families of miniature inverted-repeat transposable elements are associated with genes of the yellow fever mosquito,Aedes aegypti

“…However, the question of whether transposable elements are just ''junk'' DNA to the host, or whether they can play important and even adaptive roles in organismal evolution, is currently actively debated (e.g., refs. 6, 12, 14-17, and [55][56][57][58].…”

Drosophila melanogaster as a model for studying protein-encoding genes that are resident in constitutive heterochromatin

“…Once in heterochromatin, genes would have been targeted by recurrent insertions of transposable elements, thus generating the present structural organization. Transposable element-related sequences in heterochromatin might thus contribute, in ways that are still poorly understood, to many of the structural and functional properties of heterochromatin, including the regulatory evolution of these genes (Pimpinelli et al, 1995;Weiler and Wakimoto, 1995;Dimitri, 1997;Dimitri and Junakovic, 1999;Yasuhara et al, 2005), similar to documented instances found in euchromatin (Von Stenberg et al, 1992;Miller et al, 1999;Kidwell and Lish, 2000;Jordan et al, 2003;Brandt et al, 2005;Kapitonov and Jurka, 2005). Over evolutionary time, transposable elements can thus be viewed as 'artisans' that have shaped heterochromatin, rather than merely as parasitic sequences (Dimitri et al, 2005b).…”