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Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity.

ABSTRACT: Circadian rhythms are widespread in nature and reflect the activity of an endogenous biological clock. In metazoans, the circadian system includes a central circadian clock in the brain as well as distinct clocks in peripheral tissues such as the retina or liver. Similarly, plants have distinct clocks in different cell layers and tissues. Here, we show that two different circadian clocks, distinguishable by their sensitivity to environmental temperature signals, regulate the transcription of genes that are expressed in the Arabidopsis thaliana cotyledon. One oscillator, which regulates CAB2 expression, responds preferentially to light-dark versus temperature cycles and fails to respond to the temperature step associated with release from stratification. The second oscillator, which regulates CAT3 expression, responds preferentially to temperature versus light-dark cycles and entrains to the release from stratification. Finally, the phase response curves of these two oscillators to cold pulses are distinct. The phase response curve of the oscillator component TOC1 to cold pulses is similar to that of CAB2, indicating that CAB2 is regulated by a TOC1-containing clock. The existence of two clocks, distinguishable on the basis of their sensitivity to temperature, provides an additional means by which plants may integrate both photoperiodic and temperature signals to respond to the changing seasons.

SUBMITTER: Michael TP

PROVIDER: S-EPMC164540 | biostudies-literature | 2003 May

REPOSITORIES: biostudies-literature

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Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity.

Michael Todd P TP Salome Patrice A PA McClung C Robertson CR

Proceedings of the National Academy of Sciences of the United States of America 20030507 11

Circadian rhythms are widespread in nature and reflect the activity of an endogenous biological clock. In metazoans, the circadian system includes a central circadian clock in the brain as well as distinct clocks in peripheral tissues such as the retina or liver. Similarly, plants have distinct clocks in different cell layers and tissues. Here, we show that two different circadian clocks, distinguishable by their sensitivity to environmental temperature signals, regulate the transcription of gen ...[more]

PMID: 12736379

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Project description:Proper timing of rhythmic locomotor behavior is the consequence of integrating environmental conditions and internal time dictated by the circadian clock. Rhythmic environmental input like daily light and temperature changes (called Zeitgeber) reset the molecular clock and entrain it to the environmental time zone the organism lives in. Furthermore, depending on the absolute temperature or light intensity, flies exhibit their main locomotor activity at different times of day, i.e., environmental input not only entrains the circadian clock but also determines the phase of a certain behavior. To understand how the brain clock can distinguish between (or integrate) an entraining Zeitgeber and environmental effects on activity phase, we attempted to entrain the clock with a Zeitgeber different from the environmental input used for phasing the behavior. 150 clock neurons in the Drosophila melanogaster brain control different aspects of the daily activity rhythms and are organized in various clusters. During regular 12 h light: 12 h dark cycles at constant mild temperature (LD 25°C, LD being the Zeitgeber), so called morning oscillator (MO) neurons control the increase of locomotor activity just before lights-on, while evening oscillator (EO) neurons regulate the activity increase at the end of the day, a few hours before lights-off. Here, using 12 h: 12 h 25°C:16°C temperature cycles as Zeitgeber, we attempted to look at the impact of light on phasing locomotor behavior. While in constant light and 25°C:16°C temperature cycles (LLTC), flies show an unimodal locomotor activity peak in the evening, during the same temperature cycle, but in the absence of light (DDTC), the phase of the activity peak is shifted to the morning. Here, we show that the EO is necessary for synchronized behavior in LLTC but not for entraining the molecular clock of the other clock neuronal groups, while the MO controls synchronized morning activity in DDTC. Interestingly, our data suggest that the influence of the EO on the synchronization increases depending on the length of the photoperiod (constant light vs 12 h of light). Hence, our results show that effects of different environmental cues on clock entrainment and activity phase can be separated, allowing to decipher their integration by the circadian clock.

Project description:MotivationCircadian oscillations have been observed in animals, plants, fungi and cyanobacteria and play a fundamental role in coordinating the homeostasis and behavior of biological systems. Genetically encoded molecular clocks found in nearly every cell, based on negative transcription/translation feedback loops and involving only a dozen genes, play a central role in maintaining these oscillations. However, high-throughput gene expression experiments reveal that in a typical tissue, a much larger fraction ([Formula: see text]) of all transcripts oscillate with the day-night cycle and the oscillating species vary with tissue type suggesting that perhaps a much larger fraction of all transcripts, and perhaps also other molecular species, may bear the potential for circadian oscillations.ResultsTo better quantify the pervasiveness and plasticity of circadian oscillations, we conduct the first large-scale analysis aggregating the results of 18 circadian transcriptomic studies and 10 circadian metabolomic studies conducted in mice using different tissues and under different conditions. We find that over half of protein coding genes in the cell can produce transcripts that are circadian in at least one set of conditions and similarly for measured metabolites. Genetic or environmental perturbations can disrupt existing oscillations by changing their amplitudes and phases, suppressing them or giving rise to novel circadian oscillations. The oscillating species and their oscillations provide a characteristic signature of the physiological state of the corresponding cell/tissue. Molecular networks comprise many oscillator loops that have been sculpted by evolution over two trillion day-night cycles to have intrinsic circadian frequency. These oscillating loops are coupled by shared nodes in a large network of coupled circadian oscillators where the clock genes form a major hub. Cells can program and re-program their circadian repertoire through epigenetic and other mechanisms.Availability and implementationHigh-resolution and tissue/condition specific circadian data and networks available at http://circadiomics.igb.uci.edu.Contactpfbaldi@ics.uci.eduSupplementary informationSupplementary data are available at Bioinformatics online.

Dataset Information

Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity.

Publications

Two Arabidopsis circadian oscillators can be distinguished by differential temperature sensitivity.

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