Comparison of the oxidative phosphorylation (OXPHOS) nuclear genes in the genomes of Drosophila melanogaster, Drosophila pseudoobscura and Anopheles gambiae

Abstract

Background: In eukaryotic cells, oxidative phosphorylation (OXPHOS) uses the products of both nuclear and mitochondrial genes to generate cellular ATP. Interspecies comparative analysis of these genes, which appear to be under strong functional constraints, may shed light on the evolutionary mechanisms that act on a set of genes correlated by function and subcellular localization of their products.

Results: We have identified and annotated the Drosophila melanogaster, D. pseudoobscura and Anopheles gambiae orthologs of 78 nuclear genes encoding mitochondrial proteins involved in oxidative phosphorylation by a comparative analysis of their genomic sequences and organization. We have also identified 47 genes in these three dipteran species each of which shares significant sequence homology with one of the above-mentioned OXPHOS orthologs, and which are likely to have originated by duplication during evolution. Gene structure and intron length are essentially conserved in the three species, although gain or loss of introns is common in A. gambiae. In most tissues of D. melanogaster and A. gambiae the expression level of the duplicate gene is much lower than that of the original gene, and in D. melanogaster at least, its expression is almost always strongly testis-biased, in contrast to the soma-biased expression of the parent gene.

Conclusions: Quickly achieving an expression pattern different from the parent genes may be required for new OXPHOS gene duplicates to be maintained in the genome. This may be a general evolutionary mechanism for originating phenotypic changes that could lead to species differentiation.

Figure 1

Histogram of pairwise sequence identities between the unprocessed products of 78 orthologous D. melanogaster, D. pseudoobscura, A. gambiae and human OXPHOS genes.

Figure 2

Conservation of alternative splice variants of two OXPHOS genes in D. melanogaster, D. pseudoobscura and A. gambiae. (a,b) Schematic representation and comparison of intron-exon structure of the genes encoding the NADH ubiquinone-oxidoreductase acyl carrier protein and the ATP synthase epsilon chain in D. pseudoobscura (Dp), D. melanogaster (Dm) and A. gambiae (Ag). Coding exons are represented by red boxes and untranslated UTRs by blue boxes. Introns are not drawn to scale. Because no sufficient information is available about the transcribed non coding sequences of D. pseudoobscura, only the coding exons of the D. pseudoobscura genes are shown. mtacp1 exons duplicated in tandem are labelled 'a' and 'b'. (c) alignment of the amino-acid sequences encoded by the duplicate a and b exons of the mtacp1 gene in D. melanogaster (Dm), D. pseudoobscura (Dp), A. gambiae (Ag) and A. mellifera (Am). Residues conserved in both exons are shown in white on a black background. (d) Dendrogram showing the phylogenetic relationships between the duplicated exon DNA sequences used for the alignment shown in (c). The neighbor-joining tree derived from distance matrix analysis was constructed using MultAlin [62]. Other tree-construction methods produced similar results. PAM, percent point accepted mutations.

Figure 3

Length distribution of OXPHOS gene introns. (a) Length distribution of the 400 introns interrupting the coding sequence in the 78 D. melanogaster, D. pseudoobscura and A. gambiae OXPHOS genes investigated. (b) Comparison of the orthologous introns in the three species. Length of 138 D. melanogaster introns plotted in ascending length order was compared with the length of the 138 D. pseudoobscura orthologous introns and with the length of 98 orthologous A. gambiae introns. Note that length class shifts are rare.