Input signals to the plant circadian clock

Eukaryotes and some prokaryotes have adapted to the 24 h day/night cycle by evolving circadian clocks, which now control very many aspects of metabolism, physiology and behaviour. Circadian clocks in plants are entrained by light and temperature signals from the environment. The relative timing of internal and external events depends upon a complex interplay of interacting rhythmic controls and environmental signals, including changes in the period of the clock. Several of the phytochrome and cryptochrome photoreceptors responsible have been identified. This review concentrates on the resulting patterns of entrainment and on the multiple proposed mechanisms of light input to the circadian oscillator components.     

Functional independence of circadian clocks that regulate plant gene expression

BACKGROUND: Circadian clocks regulate the gene expression, metabolism and behaviour of most eukaryotes, controlling an orderly succession of physiological processes that are synchronised with the environmental day/night cycle. Central circadian pacemakers that control animal behaviour are located in the brains of insects and rodents, but the location of such a pacemaker has not been determined in plants. Peripheral plant and animal tissues also maintain circadian rhythms when isolated in culture, indicating that these tissues contain circadian clocks. The degree of autonomy that the multiple, peripheral circadian clocks have in the intact organism is unclear. RESULTS: We used the bioluminescent luciferase reporter gene to monitor rhythmic expression from three promoters in transgenic Arabidopsis and tobacco plants. The rhythmic expression of a single gene could be set at up to three phases in different anatomical locations of a single plant, by applying light/dark treatments to restricted tissue areas. The initial phases were stably maintained after the entraining treatments ended, indicating that the circadian oscillators in intact plants are autonomous. This result held for all the vegetative plant organs and for promoters expressed in all major cell types. The rhythms of one organ were unaffected by entrainment of the rest of the plant, indicating that phase-resetting signals are also autonomous. CONCLUSIONS: Higher plants contain a spatial array of autonomous circadian clocks that regulate gene expression without a localised pacemaker. Circadian timing in plants might be less accurate but more flexible than the vertebrate circadian system.     

Selective entrainment of the Drosophila circadian clock to daily gradients in environmental temperature

Background  

Circadian clocks are internal daily time keeping mechanisms that allow organisms to anticipate daily changes in their environment and to organize their behavior and physiology in a coherent schedule. Although circadian clocks use temperature compensation mechanisms to maintain the same pace over a range of temperatures, they are also capable of synchronizing to daily temperature cycles. This study identifies key properties of this process.     

A Plastic Clock: How Circadian Rhythms Respond to Environmental Cues in Drosophila

Circadian clocks synchronize the physiology and behavior of most animals with the day to night cycle. A fundamental property of the molecular pacemakers generating circadian rhythms is their self-sustained nature: they keep oscillating even under constant conditions, with a period close to, but not exactly, 24 h. However, circadian pacemakers have to be sensitive to environmental cues to be beneficial. They need to be reset every day to keep a proper phase relationship with the day to night cycle, and they have to be able to adjust to seasonal changes in day length and temperature. Here, we review our current knowledge of the molecular and neural mechanisms contributing to the plasticity of Drosophila circadian rhythms, which are proving to be remarkably sophisticated and complex.     

History dependence of circadian pacemaker period in the cockroach

The freerunning period of circadian clocks in constant environmental conditions can be history-dependent, and one effect of entrainment of circadian clocks by light cycles is to cause long-lasting changes in the freerunning period that are termed after-effects. We have studied after-effects of entrainment to 22-h (LD 8:14) and 26-h (LD 8:18) light cycles in the cockroach Leucophaea maderae. We find that in cockroaches, the freerunning period of the locomotor activity rhythm, measured in constant darkness (DD), is 0.7h less after entrainment to T22 than after entrainment to T26. Induction of after-effects requires several days (>1 week) entrainment, and after induction, after-effects will persist in DD for over 40 days. Further after-effects are unaltered by phase-resetting of up to 12h caused by exposure to low-temperature pulses (7 degrees C) of 24 or 48h duration. After-effects also persist through re-entrainment for 2 weeks to 24-h light cycles. These results indicate that after-effects arise from stable changes in the circadian system that are likely to be independent of phase relationships among oscillators within the circadian system. We also show that entrainment to temperature cycles does not generate after-effects indicating that light may be unique in its ability to generate lasting changes in pacemaker period.     

Cyclic Presence and Absence of Conspecifics Alters Circadian Clock Phase But Does Not Entrain the Locomotor Activity Rhythm of the Fruit Fly Drosophila melanogaster

Circadian clocks use a wide range of environmental cues, including cycles of light, temperature, food, and social interactions, to fine-tune rhythms in behavior and physiology. Although social cues have been shown to influence circadian clocks of a variety of organisms including the fruit fly Drosophila melanogaster, their mechanism of action is still unclear. Here, the authors report the results of their study aimed at investigating if daily cycles of presence and absence (PA) of conspecific male visitors are able to entrain the circadian locomotor activity rhythm of male hosts living under constant darkness (DD). The results suggest that PA cycles may not be able to entrain circadian locomotor activity rhythms of Drosophila. The outcome does not change when male hosts are presented with female visitors, suggesting that PA cycles of either sex may not be effective in bringing about stable entrainment of circadian clocks in D. melanogaster. However, in hosts whose clock phase has already been set by light/dark (LD) cycles, daily PA cycles of visitors can cause measurable change in the phase of subsequent free-running rhythms, provided that their circadian clocks are labile. Thus, the findings of this study suggest that D. melanogaster males may not be using cyclic social cues as their primary zeitgeber (time cue) for entrainment of circadian clocks, although social cues are capable of altering the phase of their circadian rhythms. (Author correspondence: vsharma@jncasr.ac.in, vksharmas@gmail.com)     

Circadian resonance in the development of two sympatric species of Camponotus ants

Circadian clocks provide adaptive advantage to their owners by timing their behavioural and physiological processes in accordance with the external environment. Here we report the results of our study aimed at investigating the effect of the interaction between circadian timing system and environmental light/dark (LD) cycles on pre-adult development time of two sympatric species of Componotus ants, the night active Componotus compressus, and the day active C. paria—both species develop in dark underground nests, under fairly constant conditions of humidity and temperature. We estimated pre-adult developmental durations in these ants under three different LD cycles (T20 = 10 h of light and 10 h of darkness, T24 = 12 h of light and 12 h of darkness, and T28 = 14 h of light and 14 h of darkness). We find that both species exhibit significantly faster pre-adult development under T24 compared to T20 and T28. Given that faster development in insects is considered as an adaptive strategy these results can be taken to suggest that Camponotus ants accrue greater fitness advantage under T24 compared to T20 and T28 LD cycles, possibly due to “circadian resonance” between circadian timing system and environmental LD cycle. Thus our study reveals that boreal species of ants could serve as a case for the study of adaptive significance of circadian organization.     

Modeling circadian clocks: Roles,advantages, and limitations

Circadian rhythms are endogenous oscillations characterized by a period of about 24h. They constitute the biological rhythms with the longest period known to be generated at the molecular level. The abundance of genetic information and the complexity of the molecular circuitry make circadian clocks a system of choice for theoretical studies. Many mathematical models have been proposed to understand the molecular regulatory mechanisms that underly these circadian oscillations and to account for their dynamic properties (temperature compensation, entrainment by light dark cycles, phase shifts by light pulses, rhythm splitting, robustness to molecular noise, intercellular synchronization). The roles and advantages of modeling are discussed and illustrated using a variety of selected examples. This survey will lead to the proposal of an integrated view of the circadian system in which various aspects (interlocked feedback loops, inter-cellular coupling, and stochasticity) should be considered together to understand the design and the dynamics of circadian clocks. Some limitations of these models are commented and challenges for the future identified.     

Plant cell responses to cold are all about timing

Changes in temperature present the cells of plants with particular challenges. Fortunately, many changes in temperature can be anticipated due to the rhythms of day/night and the seasons. To anticipate changes in the environment most organisms have a circadian clock to optimize daily and seasonal timing of gene expression, metabolism, physiology and cell biology. Circadian clocks comprised positive and negative feedback loops which ensure an internal period of approximately 24 hours. We describe the role of the circadian clock in modulating cellular cold signalling networks to prepare the cell for the onset of winter.     

Focusing on the nuclear and subnuclear dynamics of light and circadian signalling

Circadian clocks provide organisms the ability to synchronize their internal physiological responses with the external environment. This process, termed entrainment, occurs through the perception of internal and external stimuli. As with other organisms, in plants, the perception of light is a critical for the entrainment and sustainment of circadian rhythms. Red, blue, far‐red, and UV‐B light are perceived by the oscillator through the activity of photoreceptors. Four classes of photoreceptors signal to the oscillator: phytochromes, cryptochromes, UVR8, and LOV‐KELCH domain proteins. In most cases, these photoreceptors localize to the nucleus in response to light and can associate to subnuclear structures to initiate downstream signalling. In this review, we will highlight the recent advances made in understanding the mechanisms facilitating the nuclear and subnuclear localization of photoreceptors and the role these subnuclear bodies have in photoreceptor signalling, including to the oscillator. We will also highlight recent progress that has been made in understanding the regulation of the nuclear and subnuclear localization of components of the plant circadian clock.