Abstract
Color vision in Drosophila melanogaster is based on the expression of five different color-sensing Rhodopsin proteins in distinct subtypes of photoreceptor neurons. Promoter regions of less than 300 base pairs are sufficient to reproduce the unique, photoreceptor subtype-specific rhodopsin expression patterns. The underlying cis-regulatory logic remains poorly understood, but it has been proposed that the rhodopsin promoters have a bipartite structure: the distal promoter region directs the highly restricted expression in a specific photoreceptor subtype, while the proximal core promoter region provides general activation in all photoreceptors. Here, we investigate whether the rhodopsin promoters exhibit a strict specialization of their distal (subtype specificity) and proximal (general activation) promoter regions, or if both promoter regions contribute to generating the photoreceptor subtype-specific expression pattern. To distinguish between these two models, we analyze the expression patterns of a set of hybrid promoters that combine the distal promoter region of one rhodopsin with the proximal core promoter region of another rhodopsin. We find that the function of the proximal core promoter regions extends beyond providing general activation: these regions play a previously underappreciated role in generating the non-overlapping expression patterns of the different rhodopsins. Therefore, cis-regulatory motifs in both the distal and the proximal core promoter regions recruit transcription factors that generate the unique rhodopsin patterns in a combinatorial manner. We compare this combinatorial regulatory logic to the regulatory logic of olfactory receptor genes and discuss potential implications for the evolution of rhodopsins.
Highlights
A prerequisite for color vision is the expression of different wavelength-sensitive visual pigments in specific subtypes of photoreceptor neurons [1]
We study the mechanisms that control the expression of different color-sensing Rhodopsin proteins in distinct subtypes of Drosophila photoreceptors, which is the basis for color vision
We find that specific combinations of cis-regulatory motifs in the distal and the proximal core promoter regions of each rhodopsin direct its unique expression pattern
Summary
A prerequisite for color vision is the expression of different wavelength-sensitive visual pigments in specific subtypes of photoreceptor neurons [1]. The rod-equivalent Drosophila ‘outer’ PR class (R1-R6) expresses blue-green sensitive Rh1 and mediates dim light vision, while the cone-equivalent ‘inner’ PR class (R7/R8) mediates color vision (Fig 1A) [3,4]. Based on their Rh expression, the R7 and R8 PR types can be further subdivided into two subtypes, ‘p’ and ‘y’ (Fig 1A): pR7s express short UV-sensitive Rh3 and yR7s express long UV-sensitive Rh4, while pR8s express blue-sensitive Rh5 and yR8s express greensensitive Rh6 (Fig 1A, right). The transcription factor Runt has recently been identified as a novel regulator of R7 subtype specification that represses Rh4 fate, but it is unclear whether it represses Rh4 directly [15]
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