Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster.
Most organisms use 24-hr circadian clocks to keep temporal order and anticipate daily environmental changes. In Drosophila melanogaster CLOCK (CLK) and CYCLE (CYC) initiates the circadian system by promoting rhythmic transcription of hundreds of genes. However, it is still not clear whether high amp...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2014-04-01
|
| Series: | PLoS Genetics |
| Online Access: | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1004252&type=printable |
| _version_ | 1826587342514683904 |
|---|---|
| author | Ron Weiss Osnat Bartok Shaul Mezan Yuval Malka Sebastian Kadener |
| author_facet | Ron Weiss Osnat Bartok Shaul Mezan Yuval Malka Sebastian Kadener |
| author_sort | Ron Weiss |
| collection | DOAJ |
| description | Most organisms use 24-hr circadian clocks to keep temporal order and anticipate daily environmental changes. In Drosophila melanogaster CLOCK (CLK) and CYCLE (CYC) initiates the circadian system by promoting rhythmic transcription of hundreds of genes. However, it is still not clear whether high amplitude transcriptional oscillations are essential for circadian timekeeping. In order to address this issue, we generated flies in which the amplitude of CLK-driven transcription can be reduced partially (approx. 60%) or strongly (90%) without affecting the average levels of CLK-target genes. The impaired transcriptional oscillations lead to low amplitude protein oscillations that were not sufficient to drive outputs of peripheral oscillators. However, circadian rhythms in locomotor activity were resistant to partial reduction in transcriptional and protein oscillations. We found that the resilience of the brain oscillator is depending on the neuronal communication among circadian neurons in the brain. Indeed, the capacity of the brain oscillator to overcome low amplitude transcriptional oscillations depends on the action of the neuropeptide PDF and on the pdf-expressing cells having equal or higher amplitude of molecular rhythms than the rest of the circadian neuronal groups in the fly brain. Therefore, our work reveals the importance of high amplitude transcriptional oscillations for cell-autonomous circadian timekeeping. Moreover, we demonstrate that the circadian neuronal network is an essential buffering system that protects against changes in circadian transcription in the brain. |
| first_indexed | 2024-12-17T15:00:10Z |
| format | Article |
| id | doaj.art-35521a493aa1437f87a4e28b290cad09 |
| institution | Directory Open Access Journal |
| issn | 1553-7390 1553-7404 |
| language | English |
| last_indexed | 2025-03-14T16:23:55Z |
| publishDate | 2014-04-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Genetics |
| spelling | doaj.art-35521a493aa1437f87a4e28b290cad092025-02-22T05:32:00ZengPublic Library of Science (PLoS)PLoS Genetics1553-73901553-74042014-04-01104e100425210.1371/journal.pgen.1004252Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster.Ron WeissOsnat BartokShaul MezanYuval MalkaSebastian KadenerMost organisms use 24-hr circadian clocks to keep temporal order and anticipate daily environmental changes. In Drosophila melanogaster CLOCK (CLK) and CYCLE (CYC) initiates the circadian system by promoting rhythmic transcription of hundreds of genes. However, it is still not clear whether high amplitude transcriptional oscillations are essential for circadian timekeeping. In order to address this issue, we generated flies in which the amplitude of CLK-driven transcription can be reduced partially (approx. 60%) or strongly (90%) without affecting the average levels of CLK-target genes. The impaired transcriptional oscillations lead to low amplitude protein oscillations that were not sufficient to drive outputs of peripheral oscillators. However, circadian rhythms in locomotor activity were resistant to partial reduction in transcriptional and protein oscillations. We found that the resilience of the brain oscillator is depending on the neuronal communication among circadian neurons in the brain. Indeed, the capacity of the brain oscillator to overcome low amplitude transcriptional oscillations depends on the action of the neuropeptide PDF and on the pdf-expressing cells having equal or higher amplitude of molecular rhythms than the rest of the circadian neuronal groups in the fly brain. Therefore, our work reveals the importance of high amplitude transcriptional oscillations for cell-autonomous circadian timekeeping. Moreover, we demonstrate that the circadian neuronal network is an essential buffering system that protects against changes in circadian transcription in the brain.https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1004252&type=printable |
| spellingShingle | Ron Weiss Osnat Bartok Shaul Mezan Yuval Malka Sebastian Kadener Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster. PLoS Genetics |
| title | Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster. |
| title_full | Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster. |
| title_fullStr | Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster. |
| title_full_unstemmed | Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster. |
| title_short | Synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in Drosophila melanogaster. |
| title_sort | synergistic interactions between the molecular and neuronal circadian networks drive robust behavioral circadian rhythms in drosophila melanogaster |
| url | https://journals.plos.org/plosgenetics/article/file?id=10.1371/journal.pgen.1004252&type=printable |
| work_keys_str_mv | AT ronweiss synergisticinteractionsbetweenthemolecularandneuronalcircadiannetworksdriverobustbehavioralcircadianrhythmsindrosophilamelanogaster AT osnatbartok synergisticinteractionsbetweenthemolecularandneuronalcircadiannetworksdriverobustbehavioralcircadianrhythmsindrosophilamelanogaster AT shaulmezan synergisticinteractionsbetweenthemolecularandneuronalcircadiannetworksdriverobustbehavioralcircadianrhythmsindrosophilamelanogaster AT yuvalmalka synergisticinteractionsbetweenthemolecularandneuronalcircadiannetworksdriverobustbehavioralcircadianrhythmsindrosophilamelanogaster AT sebastiankadener synergisticinteractionsbetweenthemolecularandneuronalcircadiannetworksdriverobustbehavioralcircadianrhythmsindrosophilamelanogaster |