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An Ultrashort Clock Mutation at the period Locus of Drosophila melanogaster That Reveals Some New Features of the Fly's Circadian System
Ronald J. Konopka
Department of Biology, Clarkson University, Potsdam, New York 13699
Melanie J. Hamblen-Coyle
NSF Center for Biological Timing, Department of Biology, Brandeis University, Waltham, Massachusetts 02254
Creston F. Jamison
NSF Center for Biological Timing, Department of Biology, Brandeis University, Waltham, Massachusetts 02254
Jeffrey C. Hall
NSF Center for Biological Timing, Department of Biology, Brandeis University, Waltham, Massachusetts 02254
A rhythm mutant of Drosophila melanogaster was induced by chemical mutagenesis and isolated by testing for locomotor activity rhythms, which in the new variant had periods of approximately 16 hr. The sex-linked mutation responsible for this ultrashort period causes 20-hr rhythms when heterozygous with a normal X. This semidominance notwithstanding, the new mutation was revealed to be an allele of the period (per) gene by noncomplementation with per-null variants, in the sense that females heterozygous for perT (as the ultrafast-clock allele is called) and per- exhibited periods that were much shorter than in the case of perT/ +. These tests also revealed in a clearer manner than in previous cases that two "doses" of a fast-clock per mutation lead to appreciably shorter periods than those exhibited by one-dose females whose other per allele is a loss-of-function variant. In light-dark cycles (LD 12:12), flies carrying perT in a genotypic condition leading to free-running periods that are 8 hr faster than normal nevertheless entrained, by phase-shifting that large number of hours each day; the evening peak of locomotor activity was, however, many hours earlier than normal. The use of a newly developed device for monitoring Drosophila eclosion automatically showed that perT exhibits a very marginal emergence rhythm at 25°C, but periodicity of ca. 17-18 hr at 19°. Staining of the per-encoded protein (PER) in sections of perT versus normal pharate adults revealed for the first time that the immunohistochemically detected signal cycles in its intensity in wild-type, in a manner that is similar to the PER rhythm previously demonstrated in adults. The staining cycle in pharate adults expressing perT differed from that of wild-type. Temperature compensation of the adult activity rhythm of perT was found to be faulty, in that periods became appreciably shorter as the flies were heated. However, the mutant exhibited a normal degree of period lengthening when its locomotor activity was monitored in the presence of heavy water. The perT mutation interacted with the long-period Andante allele of the dusky locus in a manner that was anomalous (in comparison to dyAnd interactions with per+ or another short-period per mutation). This and other unique features of per T are discussed from the standpoint of the new mutation's heuristic value, including that which may stimulate a deeper understanding of the period gene's action at the molecular level.
Key Words: fruit flies • mutagenesis • rhythm mutants • locomotor activity • eclosion • temperature compensation • period protein cycling
Journal of Biological Rhythms, Vol. 9, No. 3-4,
189-216 (1994)
DOI: 10.1177/074873049400900303
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