Evolution of Drosophila ribosomal protein gene core promoters

Abstract

The coordinated expression of ribosomal protein genes (RPGs) has been well documented in many species. Previous analyses of RPG promoters focus only on Fungi and mammals. Recognizing this gap and using a comparative genomics approach, we utilize a motif-finding algorithm that incorporates cross-species conservation to identify several significant motifs in Drosophila RPG promoters. As a result, significant differences of the enriched motifs in RPG promoter are found among Drosophila, Fungi, and mammals, demonstrating the evolutionary dynamics of the ribosomal gene regulatory network. We also report a motif present in similar numbers of RPGs among Drosophila species which does not appear to be conserved at the individual RPG gene level. A module-wise stabilizing selection theory is proposed to explain this observation. Overall, our results provide significant insight into the fast-evolving nature of transcriptional regulation in the RPG module.

Fig. 1

The TOP sequences. TOP sequences are close to the translation start codon of ribosomal protein genes across all Drosophila species (Panel A). Here y-axis represents the number of RPG genes having TOP motif at a given distance from the translation start codon as shown in x-axis. For each ribosomal protein gene, its TOP motif is defined as the best matching sequence in the upstream 1 kb region using the estimated position weight matrix in corresponding species, which is shown in panel B.

Fig. 2

Cross-species spatial distribution of the DRE motif. DRE motifs are close to the translation start codon of ribosomal protein genes across all Drosophila species. Shown in y-axis is the number of RPGs harboring DRE in the promoter region with corresponding distance from translation start codon ATG shown in x-axis. The error bar indicated by “Random” corresponds to the null distribution of DRE in the promoter regions of all D. melanogaster genes (1000 bootstrap samples, each with 86 genes).

Fig. 3

DNA binding domain of the transcription factor DREF. The DREF DNA binding domain is conserved across Drosophila species. DNA binding domain is aligned in CLUSTALW (Higgins et al., 1994).

Fig. 4

Occurrences of DRE in the Drosophila RPG core promoters (the upstream 1 kb region of translation start codon ATG). Proteins of the large subunit are in the left panel and those of small subunit are in the right panel. Color schemes are illustrated in bottom right.