A one-day journey to the suburbs: circadian clock in the Drosophila visual system

Abstract

Living organisms, which are constantly exposed to cyclical variations in their environment, need a high degree of plasticity in their visual system to respond to daily and seasonal fluctuations in lighting conditions. In Drosophila melanogaster, the visual system is a complex tissue comprising different photoreception structures that exhibit daily rhythms in gene expression, cell morphology, and synaptic plasticity, regulated by both the central and peripheral clocks. In this review, we briefly summarize the structure of the circadian clock and the visual system in Drosophila and comprehensively describe circadian oscillations in visual structures, from molecules to behaviors, which are fundamental for the fine-tuning of visual sensitivity. We also compare some features of the rhythmicity in the visual system with that of the central pacemaker and hypothesize about the differences in the regulatory signals and mechanisms that control these two clocks.

Keywords: Drosophila; biological clocks; circadian rhythms; glia; photoreceptors; visual system.

Fig. 1

The per/tim feedback loop and role of CRY in molecular clock resetting. During the late day–early night, the dimer CLOCK (CLK)/CYCLE (CYC) activates the expression of period (per) and timeless (tim) genes. Post‐translationally modified PER and TIM proteins accumulate in the cytoplasm during the night and form heterodimers, stabilizing them and enabling their transport to the nucleus, where they inhibit their own transcription. In the presence of light, the circadian photoreceptor CRYPTOCHROME (CRY) binds TIM and promotes its proteasomal degradation through a mechanism that involves the F‐box protein JETLAG (JET). When exposed to light, CRY also becomes a substrate for JET, which initiates its ubiquitination and degradation via the proteasome.

Fig. 2

The adult Drosophila visual system. (A) The adult visual system of the fruit fly Drosophila melanogaster contains seven photoreceptive structures: two compound eyes, a pair of Hofbauer–Buchner (H‐B) eyelets, and three ocelli. (B) The compound eye is depicted in a schematic illustration, showing the retina and the four optic ganglia (lamina, medulla, lobula, and lobula plate). Within the retina, individual ommatidia accommodate photoreceptors R1–R8. In a cross‐section through the ommatidia, it is evident that the peripheral photoreceptors, R1–R6, are arranged in hexagonal patterns and cover the entire length of the retina. The inner photoreceptors, R7–R8, are situated in the center, with R7 positioned atop R8. In a cross‐section through the lamina, it can be observed that the axons of R1–R6 connect with lamina neurons to form synaptic units known as ‘cartridges’. These cartridges comprise R1–R6 input terminals and five lamina neurons (L1–L5) surrounded by glial cell processes (gl). The axons of cells R7–R8 within the inner layers extend through the lamina and end in two separate neuropil layers within the medulla.

Fig. 3

Daily rhythms of the visual system. In the compound eye, the circadian clock generates rhythms in the expression of clock and output genes, in the morphology and connections of neuronal cells and in behavior. In the HB eyelets, rhythms in output gene expression and in neuronal projections and synapses are observed. Details are provided in the main text.