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Title: Genome-Wide Analysis of Light- and Temperature-Entrained Circadian Transcripts in Caenorhabditis elegans}
Article:
Abstract:
Most organisms have an endogenous circadian clock that is synchronized to environmental signals such as light and temperature. Although circadian rhythms have been described in the nematode Caenorhabditis elegans at the behavioral level, these rhythms appear to be relatively non-robust. Moreover, in contrast to other animal models, no circadian transcriptional rhythms have been identified. Thus, whether this organism contains a bona fide circadian clock remains an open question. Here we use genome-wide expression profiling experiments to identify light- and temperature-entrained oscillating transcripts in C. elegans. These transcripts exhibit rhythmic expression with temperature-compensated 24-h periods. In addition, their expression is sustained under constant conditions, suggesting that they are under circadian regulation. Light and temperature cycles strongly drive gene expression and appear to entrain largely nonoverlapping gene sets. We show that mutations in a cyclic nucleotide-gated channel required for sensory transduction abolish both light- and temperature-entrained gene expression, implying that environmental cues act cell nonautonomously to entrain circadian rhythms. Together, these findings demonstrate circadian-regulated transcriptional rhythms in C. elegans and suggest that further analyses in this organism will provide new information about the evolution and function of this biological clock.
Introduction:
Organisms exhibit daily( circadian) rhythms in behavior and physiology that are attuned to the earth's rotational period. The periods of these intrinsic rhythms are approximately 24 h and are synchronized by external cues or zeitgebers( time givers) such as light and temperature. The molecular composition and regulation of endogenous pacemakers that generate circadian rhythms have been extensively investigated. Both the molecules composing the core clock and the molecular mechanisms of clock function are remarkably divergent across kingdoms, as well as between eukaryotes and prokaryotes, suggesting multiple, independent evolutionary origins for the circadian clock[1]–[6]. However, genes and pathways by which circadian oscillatory rhythms are generated in animals such as Drosophila and mammals are strongly conserved[5],[7],[8], implying a single origin of the clock in the metazoan lineage[2]. Thus, it is of interest to identify and characterize the circadian clock in additional animals. The nematode Caenorhabditis elegans is well established as an excellent model organism for the study of development and behavior[9]–[12]. In their soil habitat, worms are subjected to temperature fluctuations corresponding to solar irradiance during the day–night cycles[13],[14]. Moreover, when associated with surface-dwelling animals[15], C. elegans is likely to be exposed to daily light–dark cycles. Several studies have previously reported the presence of circadian rhythms in C. elegans. In these studies, growth-synchronized populations were entrained to light or temperature cycles, and circadian rhythms in behaviors such as locomotion or responses to osmotic stress were quantified[16]–[20]. Although these experiments demonstrated the presence of rhythms with characteristics of true circadian oscillations, these rhythms were surprisingly variable and non-robust[19]. In addition, while the C. elegans genome is predicted to encode homologs of most Drosophila and mammalian core clock components, the roles of these genes appear to be largely restricted to development[21]. Thus, whether C. elegans exhibits bona fide circadian rhythms remains unclear. Circadian rhythmicity in behavior and physiology has been proposed to be driven by clock-regulated oscillations in transcription and translation, and/or via post-transcriptional or post-translational modifications[22]–[32]. The expression of core clock genes such as per( period) and tim( timeless) as well as many clock output genes cycles at the transcriptional level in a circadian manner in Drosophila[23],[24]. Expression profiling experiments have, therefore, provided a powerful approach to identify clock genes as well as clock output genes under circadian transcriptional control[33]–[41]. Since expression profiling is not biased by prior assumptions regarding a specific behavioral or physiological output, transcriptional rhythms may be a robust measure of the presence of a molecular circadian clock. Here we identify light- and temperature-regulated transcriptional rhythms in C. elegans and show that subsets of these transcripts are regulated in a circadian manner. We find that light and temperature also globally drive the expression of many genes, indicating that C. elegans exhibits systemic responses to these stimuli. Light- and temperature-entrained transcripts appear to be largely nonoverlapping. We show that conserved clock gene homologs do not exhibit circadian rhythmicity at the mRNA level. We also find that the TAX-2 cyclic nucleotide-gated channel subunit, previously implicated in thermosensory signal transduction and phototransduction[42]–[44] is required to transduce both light and temperature information to the clock( s). These results demonstrate that C. elegans has circadian clock( s) that are entrained by light and temperature, and indicate that this model organism can be used to further explore the evolution and function of this critical timekeeping mechanism.
Discussion:
In the present study, we report the first identification, to our knowledge, of circadian-regulated transcripts in C. elegans. These transcripts are entrained by LD or WC cycles and continue to oscillate during free-running conditions with temperature-compensated periods and phases that are dependent on entraining conditions. Both light and temperature can act as zeitgebers, and they drive as well as entrain transcripts at the genome-wide level. Genome-wide circadian expression is regulated by environmental information received by a small set of sensory neuron( s), suggesting that, similar to observations in vertebrates, light and temperature information may act cell-nonautonomously to entrain the clock( s) in C. elegans. Our findings also imply that C. elegans may utilize a timekeeping mechanism that is distinct from that described previously in other animals. In C. elegans, as well as in Drosophila, temperature cycles drive the expression of a larger set of genes than do light cycles[41],[47]. Genes implicated in metabolism appear to be enriched in the temperature-driven transcript sets, whereas genes implicated in circadian behaviors such as locomotion and reproduction are enriched in the entrained datasets in both organisms([47] and this study). However, there is a surprising lack of overlap between the temperature- and light-entrained datasets in C. elegans. In contrast, in Drosophila, light and temperature cooperatively entrain a single transcriptional clock[47],. What does this almost complete lack of overlap between the two C. elegans entrained datasets imply? At one extreme, light and temperature might act via different mechanisms to entrain two distinct clocks. Multiple clocks within a single organism are not unprecedented[4], although there is no evidence for a similar situation in metazoans. On the contrary, Drosophila has only a single clock that runs in multiple cells and tissues[47],[69]. Similarly, C. elegans may have a single clock that is entrained by light or temperature in different tissues. In this scenario, the different locations may have completely distinct sets of output genes, accounting for the nonoverlapping datasets. However, in this case, cycling clock mRNAs are expected to be shared in common between the two sets since in all eukaryotic circadian systems, from plants to mammals, many clock mRNAs undergo circadian oscillations at the transcriptional level[23],[24],[71],[72]. Since it is unlikely that a clock based on transcriptional feedback loops would have only one cycling mRNA( e. g., the swd-3. 3 gene), C. elegans may have a novel clock mechanism. Consistent with this hypothesis, homologs of animal clock genes do not cycle in C. elegans. Recent analysis has suggested that the ascidian Ciona intestinalis also has a divergent circadian clock, further suggesting multiple evolutionary origins of the animal circadian mechanism[73]. However, it remains possible that cycling clock mRNAs were not identified in our genome-wide studies because of masking by noncycling expression in other tissue types, or that clock proteins exhibit functional rhythmicity in C. elegans via post-translational modifications[74]–[76]. An alternative possibility, consistent with the presence of a single clock, is that cycling clock mRNAs as well as common output genes are present in the two driven datasets. These datasets have a statistically significant overlap, which is expected for clock and clock-regulated mRNAs. However, these transcripts do not appear to maintain cycling in free-running conditions. Although free-running rhythms are considered to be the sine qua non for circadian genes, some bona fide circadian rhythms damp quickly in constant conditions. For example, Drosophila peripheral rhythms damp rapidly in the absence of a light–dark cycle, including transcriptional rhythms of the clock genes themselves[77],[78]. Consistent with this scenario, we identified one of seven examined transcripts in the WC-driven datasets with characteristics of an entrained rather than a strictly driven transcript. The number of entrained transcripts is, therefore, likely to be larger, and both clock mRNAs and shared output genes may be present within the set of entrained genes whose expression is severely dampened under constant conditions. Further molecular and genetic analyses will allow us to distinguish among the above possibilities. What are the behavioral consequences of circadian rhythmicity in C. elegans? Although locomotion has been reported to be under circadian control and genes implicated in locomotor behaviors are enriched in the WC-entrained dataset, this behavioral output does not appear to be particularly robust, and exhibits marked animal-to-animal variability[16],[19]. Locomotor behaviors in C. elegans are complex and can be dissected into multiple behavioral components[79]–[83]. Reported analyses of circadian locomotor behavior relied largely on quantification of gross overall movement[16],[18], suggesting that detailed analyses of the underlying components may reveal more robust clock control. Since reproduction-related genes are also enriched in the entrained datasets, additional biologically relevant behaviors such as egg-laying or mating may also be regulated in a circadian manner in C. elegans. Identification of circadian transcriptional rhythms in C. elegans now provides the necessary reagents to characterize the molecular identity, the neuronal circuits, and the behavioral consequences of clock function in this important model organism.
Daily ( circadian ) rhythms in behavior and physiology allow organisms to adapt to periodic cues such as light and temperature associated with the rotation of the earth . Subsets of molecular components of the internal clock that drive these rhythms , as well as effector genes for behavioral outputs , also exhibit rhythmic expression in many organisms . While circadian rhythms in behavior have previously been described in the nematode Caenorhabditis elegans , no transcriptional rhythms or clock genes have been identified , leaving open the question of the nature of the clock in this organism . Here , we identify light- and temperature-entrained cycling genes in C . elegans via genome-wide transcriptional profiling . Transcripts showing circadian regulation ( including expression with a 24-h period maintained upon removal of the entraining stimulus ) and temperature compensation were identified . Light and temperature appear to entrain independent sets of genes . We also identify large sets of light- or temperature-driven genes . Mutations in a channel gene previously implicated in sensory transduction in a small set of sensory neurons abolish entrainment of gene expression by environmental signals . This work demonstrates the presence of circadian transcriptional rhythms in C . elegans , and provides the foundation for future investigations into the underlying mechanisms .