Evolution of Gene Sequence in Response to Chromosomal Location

Abstract

Evolutionary forces acting on the repetitive DNA of heterochromatin are not constrained by the same considerations that apply to protein-coding genes. Consequently, such sequences are subject to rapid evolutionary change. By examining the Troponin C gene family of Drosophila melanogaster, which has euchromatic and heterochromatic members, we find that protein-coding genes also evolve in response to their chromosomal location. The heterochromatic members of the family show a reduced CG content and increased variation in DNA sequence. We show that the CG reduction applies broadly to the protein-coding sequences of genes located at the heterochromatin:euchromatin interface, with a very strong correlation between CG content and the distance from centric heterochromatin. We also observe a similar trend in the transition from telomeric heterochromatin to euchromatin. We propose that the methylation of DNA is one of the forces driving this sequence evolution.

Silent but Not Static: Accelerated Base-Pair Substitution in Silenced Chromatin of Budding Yeasts

“…Two recent studies indicate an elevated substitution rate in X chromosome subtelomeric regions and Troponin C gene family members of Drosophila melanogaster [34],[35]. Our study established the generality of this effect across taxa, extended it to the full genome analysis, and excluded all proposed mechanisms except for elevated mutation in silenced regions.…”

Birth of a new gene on the Y chromosome ofDrosophila melanogaster

“…S3). This substitution bias is the probable cause of the previously found pattern that Drosophila heterochromatic genes in general (including Y-linked ones) are AT rich (33,34). Unfortunately all available codon substitution models assume stationary base composition, and it has been shown that they are sensitive to violations of this assumption (35).…”

Essential Loci in Centromeric Heterochromatin of Drosophila melanogaster. I: The Right Arm of Chromosome 2

“…One of the main distinguishing features of heterochromatin is the high density of repeat sequences (Gatti and Pimpinelli 1992;Lohe et al 1993;Bartolomé et al 2002); in fact, it has been shown that some heterochromatic genes are located within regions containing nearly 90% repeats, including transposable element and repetitive satellite sequences (Smith et al 2007). In addition, heterochromatic genes generally possess larger introns consisting mainly of transposable element remnants (Devlin et al 1990;Uchida et al 1993;Biggs et al 1994;Tulin et al 2002;Dimitri et al 2003b;Smith et al 2007) and are often enriched in terms of AT content (Adams et al 2000;Díaz-Castillo and Golic 2007).…”

“…On average, heterochromatic genes are larger than euchromatic genes, primarily due to the prevalent accumulation of transposable element sequences in their introns (Devlin et al 1990;Biggs et al 1994;Dimitri et al 2003a,b;Hoskins et al 2007). Heterochromatic genes also tend to be AT-rich compared to their euchromatic counterparts; there is some evidence suggesting that the coding sequences of heterochromatic genes evolve toward AT richness in response to being located in heterochromatin (Yasuhara et al 2005;Díaz-Castillo and Golic 2007).…”