Epigenetics and Codon Usage of the Histone Genes in 12 Drosophila Species

Abstract

Histones are proteins that bind to DNA and form nucleosomes. There are several types of histones that differ in chromosome distribution and timing of their expression. In Drosophila, each canonical type histone is identical or highly similar in amino acid sequence to its corresponding replacement type histone; however, gene structure and codon usage differ between the two types of histones. Identification of the evolutionary changes responsible for the differences between these two histone types will lead to an understanding of the development of epigenetic regulation. Here, recent findings regarding codon usage for canonical and replacement types of histones are outlined for study of the evolution of these histone genes and their epigenetic regulation in Drosophila.

The Adenine/Thymine Deleterious Selection Model for GC Content Evolution at the Third Codon Position of the Histone Genes in Drosophila

“…The positive relationship found between codon bias and the level of gene expression most likely resulted from the difference in translation efficiency [ 45 , 46 ]. Among the canonical histone genes, H2B showed the highest GC content at the third codon position, while H1 showed the lowest GC content at the third codon position [ 62 ]. H1, a linker protein, is expressed at approximately half of the level of the other four canonical histones.…”

“…A comparison of the average GC content at the third codon position of genes in 12 common species revealed a higher GC content at the third codon position in the genes of the replacement type of histones than in those of the canonical type of histones [ 62 , 63 , 64 , 65 ]. Analysis of codon bias in the histone genes demonstrated that the difference was caused not by an obvious codon bias in a specific amino acid but by a general tendency that was observed for many codons [ 62 ]. Differences in functional differentiation or translation efficiency may be the cause of the differences in GC content at the third codon position between the histone types.…”

“…Although variability in the GC content among the genes within a species has been previously noted [ 36 , 40 , 50 , 51 ], variability has also been observed between different species [ 40 , 51 , 62 ]. For example, among 12 Drosophila species, the GC content at the third codon position of many genes in Drosophila willistoni was relatively lower than in the other 11 species [ 39 , 62 ]. Furthermore, when the GC content at the third codon position of corresponding genes was compared between the Drosophila species, nearly parallel differences, similar patterns of ups and downs, were observed for most comparisons ( Figure 2 ).…”

“…The differences in GC content at the third codon position according to the Drosophila phylogeny were unexpected and lacked consistency with evolution [ 33 , 62 ]. The GC contents at the third codon position of closely related species showed similar values, but those in distantly related species did not always show larger differences.…”

“…In most cases, these regions are observed to be AT rich, meaning that the mutation is biased for adenine/thymine (A/T) [ 40 , 41 ]. For example, in the D. melanogaster histone gene cluster, the GC content of the longest spacer between the H1–H3 genes was observed to be the lowest at 30% [ 31 , 32 , 62 ]. Therefore, a mutation in D. melanogaster must be biased, at least a little, for A/T.…”