Circadian clocks in antennal neurons are necessary and sufficient for olfaction rhythms in Drosophila.
BACKGROUND
The Drosophila circadian clock is controlled by interlocked transcriptional feedback loops that operate in many neuronal and nonneuronal tissues. These clocks are roughly divided into a central clock, which resides in the brain and is known to control rhythms in locomotor activity, and peripheral clocks, which comprise all other clock tissues and are thought to control other rhythmic outputs. We previously showed that peripheral oscillators are required to mediate rhythmic olfactory responses in the antenna, but the identity and relative autonomy of these peripheral oscillators has not been defined.


RESULTS
Targeted ablation of lateral neurons by using apoptosis-promoting factors and targeted clock disruption in antennal neurons with newly developed dominant-negative versions of CLOCK and CYCLE show that antennal neurons, but not central clock cells, are necessary for olfactory rhythms. Targeted rescue of antennal neuron oscillators in cyc(01) flies through wild-type CYCLE shows that these neurons are also sufficient for olfaction rhythms.


CONCLUSIONS
Antennal neurons are both necessary and sufficient for olfaction rhythms, which demonstrates for the first time that a peripheral tissue can function as an autonomous pacemaker in Drosophila. These results reveal fundamental differences in the function and organization of circadian oscillators in Drosophila and mammals and suggest that components of the olfactory signal transduction cascade could be targets of circadian regulation.
Tanoue
Shintaro
S
Department of Biology and Biochemistry, University of Houston, 4800 Calhoun Road, Houston, TX 77204 USA.
Krishnan
Parthasarathy
P
Krishnan
Balaji
B
Dryer
Stuart E
SE
Hardin
Paul E
PE
D056930:ARNTL Transcription Factors; D000704:Analysis of Variance; D000818:Animals; D030801:Animals, Genetically Modified; D051792:Basic Helix-Loop-Helix Proteins; D001683:Biological Clocks / Q000502:physiology*; D056926:CLOCK Proteins; D002940:Circadian Rhythm / Q000235:genetics / Q000502:physiology*; D017931:DNA Primers; D004330:Drosophila / Q000235:genetics / Q000502:physiology*; D029721:Drosophila Proteins / Q000502:physiology; D004594:Electrophysiology; D005246:Feedback; D005786:Gene Expression Regulation / Q000502:physiology*; D008156:Luciferases; D009043:Motor Activity / Q000502:physiology; D009475:Neurons, Afferent / Q000378:metabolism / Q000502:physiology*; D009812:Odorants; D010957:Plasmids / Q000235:genetics; D012333:RNA, Messenger / Q000378:metabolism; D012903:Smell / Q000502:physiology*; D015534:Trans-Activators / Q000502:physiology; D014157:Transcription Factors / Q000502:physiology; D019076:Transgenes
D056930:ARNTL Transcription Factors; D051792:Basic Helix-Loop-Helix Proteins; D056926:CLOCK Proteins; D017931:DNA Primers; D029721:Drosophila Proteins; D008156:Luciferases; D012333:RNA, Messenger; D015534:Trans-Activators; D014157:Transcription Factors; C120526:Clk protein, Drosophila; C112805:cyc protein, Drosophila