Abstract
The photoreceptors of the Drosophila compound eye are a classical model for studying cell fate specification. Photoreceptors (PRs) are organized in bundles of eight cells with two major types – inner PRs involved in color vision and outer PRs involved in motion detection. In wild type flies, most PRs express a single type of Rhodopsin (Rh): inner PRs express either Rh3, Rh4, Rh5 or Rh6 and outer PRs express Rh1. In outer PRs, the K50 homeodomain protein Dve is a key repressor that acts to ensure exclusive Rh expression. Loss of Dve results in de-repression of Rhodopsins in outer PRs, and leads to a wide distribution of expression levels. To quantify these effects, we introduce an automated image analysis method to measure Rhodopsin levels at the single cell level in 3D confocal stacks. Our sensitive methodology reveals cell-specific differences in Rhodopsin distributions among the outer PRs, observed over a developmental time course. We show that Rhodopsin distributions are consistent with a two-state model of gene expression, in which cells can be in either high or basal states of Rhodopsin production. Our model identifies a significant role of post-transcriptional regulation in establishing the two distinct states. The timescale for interconversion between basal and high states is shown to be on the order of days. Our results indicate that even in the absence of Dve, the Rhodopsin regulatory network can maintain highly stable states. We propose that the role of Dve in outer PRs is to buffer against rare fluctuations in this network.
Highlights
The ability of Drosophila to perceive color and motion depends on the specific patterning of several Rhodopsin proteins throughout its retina [1,2,3]
One of the bestcharacterized networks governs the development of the fruit-fly retina, a highly organized, three-dimensional organ composed of a hexagonal grid of eight types of photoreceptor neurons
Using mathematical models of gene expression, we attribute this variability to stochastic events that activate Rhodopsin production
Summary
The ability of Drosophila to perceive color and motion depends on the specific patterning of several Rhodopsin proteins throughout its retina [1,2,3]. The fly retina is a complex threedimensional structure that consists of a lattice of approximately 800 simple eyes known as ommatidia [4]. Beginning at the third instar larva, photoreceptors arise following the passage of a morphogenetic furrow across the eye imaginal disc, a monolayer of epithelial cells. Cells are recruited to ommatidia in a stereotyped manner wherein the R8 photoreceptor is recruited first and followed by pairs of outer photoreceptors: R2 and R5, R3 and R4, R1 and R6. Photoreceptors express specific Rhodopsins (for details of the process, see [13,14])
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