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The Journal of Neuroscience, November 1, 2002, 22(21):9255-9266
The Extraretinal Eyelet of Drosophila: Development, Ultrastructure, and Putative Circadian Function
Charlotte Helfrich-Förster1, 2, Tara Edwards3, Kouji Yasuyama4, Barbara Wisotzki2, Stephan Schneuwly2, Ralf Stanewsky2, Ian A. Meinertzhagen3, and Alois Hofbauer2 1 Zoological Institute/Animal Physiology, University of Tübingen, D-72076 Tübingen, Germany, 2 Zoological Institute, University of Regensburg, D-93040 Regensburg, Germany, 3 Life Sciences Centre, Dalhousie University, Halifax, Nova Scotia, Canada B3H 4J1, and 4 Department of Biology, Kawasaki Medical School, Kurashiki City, Okayama, 701-0192, Japan
Circadian rhythms can be entrained by light to follow the daily solar cycle. In Drosophila melanogaster a pair of extraretinal eyelets expressing immunoreactivity to Rhodopsin 6 each contains four photoreceptors located beneath the posterior margin of the compound eye. Their axons project to the region of the pacemaker center in the brain with a trajectory resembling that of Bolwig's organ, the visual organ of the larva. A lacZ reporter line driven by an upstream fragment of the developmental gap gene Krüppel is a specific enhancer element for Bolwig's organ. Expression of immunoreactivity to the product of lacZ in Bolwig's organ persists through pupal metamorphosis and survives in the adult eyelet. We thus demonstrate that eyelet derives from the 12 photoreceptors of Bolwig's organ, which entrain circadian rhythmicity in the larva. Double labeling with anti-pigment-dispersing hormone shows that the terminals of Bolwig's nerve differentiate during metamorphosis in close temporal and spatial relationship to the ventral lateral neurons (LNv), which are essential to express circadian rhythmicity in the adult. Bolwig's organ also expresses immunoreactivity to Rhodopsin 6, which thus continues in eyelet. We compared action spectra of entrainment in different fly strains: in flies lacking compound eyes but retaining eyelet (so1), lacking both compound eyes and eyelet (so1;gl60j), and retaining eyelet but lacking compound eyes as well as cryptochrome (so1;cryb). Responses to phase shifts suggest that, in the absence of compound eyes, eyelet together with cryptochrome mainly mediates phase delays. Thus a functional role in circadian entrainment first found in Bolwig's organ in the larva is retained in eyelet, the adult remnant of Bolwig's organ, even in the face of metamorphic restructuring.
Key words: Drosophila melanogaster; circadian rhythm; Bolwig's organ; extraretinal photoreceptors; compound eye; insect; rhodopsin
Copyright © 2002 Society for Neuroscience 0270-6474/02/22219255-12$05.00/0
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