Assessing the influence of adjacent gene orientation on the evolution of gene upstream regions in Arabidopsis thaliana

Abstract

The orientation of flanking genes may influence the evolution of intergenic regions in which cis-regulatory elements are likely to be located: divergently transcribed genes share their 5' regions, resulting either in smaller "private" spaces or in overlapping regulatory elements. Thus, upstream sequences of divergently transcribed genes (bi-directional upstream regions, or URs) may be more constrained than those of uni-directional gene pairs. We investigated this effect by analyzing nucleotide variation segregating within and between Arabidopsis species. Compared to uni-directional URs, bi-directional URs indeed display lower population mutation rate, as well as more low-frequency polymorphisms. Furthermore, we find that bi-directional regions undergo selection for the maintenance of intergenic distance. Altogether, however, we observe considerable variation in evolutionary rates, with putative signatures of selection on two uni-directional upstream regions.

Figure 1.—

Schematic of the two classes of upstream regions (URs). Shaded block arrows represent open reading frames along the chromosome and thin solid arrows represent transcription start sites. Uni-directional URs (A) are encoded on the same DNA strand. Bi-directional URs (B) are located between two start codons.

Figure 2.—

Indel polymorphism and intergenic distance. Short bi-directional URs have a significantly lower level of indel polymorphism (two-way ANOVA: F_1,25 = 6.755, P < 0.01546).