Rate of promoter class turn-over in yeast evolution

Abstract

Background: Phylogenetic conservation at the DNA level is routinely used as evidence of molecular function, under the assumption that locations and sequences of functional DNA segments remain invariant in evolution. In particular, short DNA segments participating in initiation and regulation of transcription are often conserved between related species. However, transcription of a gene can evolve, and this evolution may involve changes of even such conservative DNA segments. Genes of yeast Saccharomyces have promoters of two classes, class 1 (TATA-containing) and class 2 (non-TATA-containing).

Results: Comparison of upstream non-coding regions of orthologous genes from the five species of Saccharomyces sensu stricto group shows that among 212 genes which very likely have class 1 promoters in S. cerevisiae, 17 probably have class 2 promoters in one or more other species. Conversely, among 322 genes which very likely have class 2 promoters in S. cerevisiae, 44 probably have class 1 promoters in one or more other species. Also, for at least 2 genes from the set of 212 S. cerevisiae genes with class 1 promoters, the locations of the TATA consensus sequences are substantially different between the species.

Conclusion: Our results indicate that, in the course of yeast evolution, a promoter switches its class with the probability at least approximately 0.1 per time required for the accumulation of one nucleotide substitution at a non-coding site. Thus, key sequences involved in initiation of transcription evolve with substantial rates in yeast.

Figure 1

Average per-nucleotide conservation of TATA box and of 10 nucleotides to its left and right. Conservation of all four non-cerevisiae species is pooled together. Grey shading, TATA box; blue solid line, genes sensitive to mutations in DNA binding surface of TBP (N = 213); red dashed line, genes insensitive to mutations in DNA binding surface of TBP (N = 34).

Figure 2

Switch of promoter type by ABZ1 gene. Red, TATA consensus sequence; green, ATG start codon. S. cerevisiae carries the consensus TATA(T/A)A(T/A)(T/G) sequence in position -73 relative to the ATG start codon. The consensus is also conserved in S. paradoxus, S. kudriavtsevii and S. bayanus. In S. mikatae, at least two nucleotides are substituted, eliminating the TATA box.

Figure 3

Genes with functional class 1 (TATA box-containing) promoters in S. cerevisiae in which TATA box shifted in one of the other species of sensu stricto group. Red, TATA consensus sequence; green, ATG start codon. In ORF YFR055W (hypothetical ORF), the distance in alignment between starts of TATA consensus sequences in S. cerevisiae and S. bayanus is 17 nucleotides. In ORF YBR145W (ADH5, alcohol dehydrogenase isoenzyme), the distance in alignment between starts of TATA consensus sequences in S. cerevisiae and S. bayanus is 19 nucleotides.