Insect photoperiodism: seeing the light

This review examines the spectral sensitivities of photoperiodic responses in insects and mites in relation to circadian‐based models for the photoperiodic clock. It concludes that there are probably a number of different photoreceptors at both the organ and molecular levels. These latter probably fall into two classes: (i) a blue‐light sensitive photoreceptor and (ii) a range of opsins (i.e. opsin proteins conjugated with a vitamin A based pigment) absorbing light at a range of wavelengths. In flesh flies (Sarcophaga spp. and possibly other higher Diptera), which are considered to exemplify the ‘external coincidence’ model, entrainment of the photoperiodic oscillator probably involves a blue‐light photoreceptor of Drosophila‐type CRYPTOCHROME (CRY1) absorbing maximally at approximately 470 nm, whereas opsins absorbing at longer wavelengths may be involved in the photo‐inductive process (diapause/nondiapause regulation) that occurs when dawn light coincides with the photo‐inducible phase. In the parasitic wasp Nasonia vitripennis, on the other hand, a species that lacks CRY1 but expresses the nonphotosensitive ‘mammalian‐type’ CRY2, and is considered to exemplify ‘internal coincidence’, entrainment of the dawn and dusk oscillators may involve opsin‐based photoreceptors absorbing light at longer wavelengths as far as the red end of the spectrum. In the Lepidoptera, which express both CRY1 and CRY2, properties of both external and internal coincidence may be evident. The presence or absence of cry1 in the genome may thus emerge as a key to the photoperiodic mechanism on its light input pathway.     

Circadian organization in Aplysia californica.

Substantial progress has been made in unraveling the organization of the circadian system of Aplysia californica. There are at least three circadian pacemakers in Aplysia. One has been localized in each eye and a third lies outside the eyes. Removal of the eyes disrupts the free-running locomotor activity rhythm; however, an extraocular oscillator can mediate a free-running rhythm in some eyeless animals. Although photoreceptors sufficient for entrainment of the ocular oscillator have been localized in the retina, photoreceptors outside the eyes are capable of "driving" a diurnal rhythm of locomotor activity and may also influence entrainment of ocular pacemakers. Finally, attention has been focused on the optic nerve as a coupling pathway between various parts of the system. The evidence suggests that information transmitted in the optic nerves is involved in entrainment of the ocular pacemaker by light, and in ocular control of the locomotor activity rhythm.     

What makes the Arabidopsis clock tick on time? A review on entrainment

Entrainment, the synchronization of a circadian clock with the external environment, is a crucial step in daily life. Although many signals contribute to entrainment, light and temperature are typically the strongest resetting cues. Much progress has been made concerning light resetting in the model plant Arabidopsis thaliana. Multiple photoreceptors (phytochromes, cryptochromes, LOV-domain proteins) are involved in light perception. The clock genes CCA1, LHY and TOC1 are all probable targets of light signalling, although the details of these pathways are not completely established. Temperature can entrain the clock, but little is known about the mechanism underlying this resetting; no obvious clock gene candidate for temperature resetting has been identified. Although circadian research has emphasized oscillations in free-running conditions, in the real world the circadian clock is entrained. During entrainment, short or long period mutants exhibit a 24-h period, but a mutant phenotype is often manifested as an altered phase relationship with the entraining cycle; short and long period mutants show leading and lagging phases, respectively, and this may be detrimental under some conditions. Arrhythmic CCA1-overexpressing plants display increased lethality under very short photoperiods, consistent with the circadian clock being of adaptive significance to life on a rotating world.     

Modeling the role of mid-wavelength cones in circadian responses to light

Nonvisual responses to light, such as photic entrainment of the circadian clock, involve intrinsically light-sensitive melanopsin-expressing ganglion cells as well as rod and cone photoreceptors. However, previous studies have been unable to demonstrate a specific contribution of cones in the photic control of circadian responses to light. Using a mouse model that specifically lacks mid-wavelength (MW) cones we show that these photoreceptors play a significant role in light entrainment and in phase shifting of the circadian oscillator. The contribution of MW cones is mainly observed for light exposures of short duration and toward the longer wavelength region of the spectrum, consistent with the known properties of this opsin. Modeling the contributions of the various photoreceptors stresses the importance of considering the particular spectral, temporal, and irradiance response domains of the photopigments when assessing their role and contribution in circadian responses to light.     

A Novel Cryptochrome-Dependent Oscillator in Neurospora crassa

Several lines of evidence suggest that the circadian clock is constructed of multiple molecular feedback oscillators that function to generate robust rhythms in organisms. However, while core oscillator mechanisms driving specific behaviors are well described in several model systems, the nature of other potential circadian oscillators is not understood. Using genetic approaches in the fungus Neurospora crassa, we uncovered an oscillator mechanism that drives rhythmic spore development in the absence of the well-characterized FRQ/WCC oscillator (FWO) and in constant light, conditions under which the FWO is not functional. While this novel oscillator does not require the FWO for activity, it does require the blue-light photoreceptor CRYPTOCHROME (CRY); thus, we call it the CRY-dependent oscillator (CDO). The CDO was uncovered in a strain carrying a mutation in cog-1 (cry-dependent oscillator gate-1), has a period of ∼1 day in constant light, and is temperature-compensated. In addition, cog-1 cells lacking the circadian blue-light photoreceptor WC-1 respond to blue light, suggesting that alternate light inputs function in cog-1 mutant cells. We show that the blue-light photoreceptors VIVID and CRY compensate for each other and for WC-1 in CRY-dependent oscillator light responses, but that WC-1 is necessary for circadian light entrainment.     

A role for cyclic AMP in entrainment of the circadian oscillator in Xenopus retinal photoreceptors by dopamine but not by light

The circadian oscillator in Xenopus retinal photoreceptor layers can be reset in similar ways by light and agonists of D2-like dopamine receptors. Treatments that increase cyclic AMP levels act on this oscillator in an opposite fashion, mimicking darkness in the induction of phase shifts. Light and dopamine have each been reported to inhibit adenylate cyclase in photoreceptors. Together, these data suggest that the transduction pathways for entrainment by dopamine and/or light include suppression of cyclic AMP or a cyclic AMP-sensitive step. In these studies, we examined this hypothesis by measuring the effects of treatment with a cyclic AMP analogue on the phase shifts induced in photoreceptor melatonin rhythms by light or a D2 receptor agonist (quinpirole). When photoreceptor layers were treated simultaneously with 8-(4-chlorophenylthio)cyclic AMP (8-CPT-cAMP) and quinpirole at any of three different phases of the circadian cycle, the resulting phase shifts of the melatonin rhythm were always the same as those caused by 8-CPT-cAMP alone. This indicates that there is a cyclic AMP-sensitive step in the dopamine entrainment pathway. In contrast, light pulses did reset the oscillator in the presence of elevated cyclic AMP. This suggests a separate cyclic AMP-insensitive transduction pathway for entrainment by light. Quinpirole reduced basal levels of cyclic AMP in photoreceptors, but light did not. These data suggest that cyclic AMP plays a role in the entrainment pathway activated by dopamine but not in the entrainment pathway activated by light.     

A suite of photoreceptors entrains the plant circadian clock

Circadian rhythms in plants are relatively robust, as they are maintained both in constant light of high fluence rates and in darkness. Plant circadian clocks exhibit the expected modes of photoentrainment, including period modulation by ambient light and phase resetting by brief light pulses. Several of the phytochrome and cryptochrome photoreceptors responsible have been studied in detail. This review concentrates on the resulting patterns of entrainment and on the multiple proposed mechanisms of light input to the circadian oscillator components.     

Cyclic AMP Resets the Circadian Clock in Cultured Xenopus Retinal Photoreceptor Layers

Abstract: The Xenopus retinal photoreceptor layer contains a circadian oscillator that regulates melatonin synthesis in vitro. The phase of this oscillator can be reset by light or dopamine. The phase-response curves for light and dopamine are similar, with transitions from phase delays to phase advances in the mid-subjective night. Light and dopamine each can inhibit adenylate cyclase in retinal photoreceptors, suggesting cyclic AMP as a candidate second messenger for entrainment of the circadian oscillator. We report here that treatments that increase intracellular cyclic AMP reset the phase of the photoreceptor circadian oscillator, and that the phase-response curves for these treatments are 180° out of phase with the phase-response curves for light and dopamine. Activation of adenylate cyclase by forskolin during the late subjective day or early subjective night caused phase advances. The same treatment during the late subjective night or early subjective day caused phase delays. Similar phase shifts were induced by 3-isobutyl-1-methyl-xanthine (a phosphodiesterase inhibitor) or 8-(4-chlorophenylthio)cyclic AMP. All of these treatments also acutely increased melatonin release. Forskolin and 3-isobutyl-1-methylxanthine increased the accumulation of intracellular cyclic AMP, but not cyclic GMP, in photoreceptor layers. The results indicate that cyclic AMP-dependent pathways regulate the photoreceptor circadian oscillator and suggest that a decrease in cyclic AMP may be involved in circadian entrainment by light and/or dopamine.     

Cryptochromes integrate green light signals into the circadian system

Plants are acutely sensitive of their light environment, adapting their growth habit and prioritizing developmental decisions to maximize fecundity. In addition to providing an energy source and directional information, light quality also contributes to entrainment of the circadian system, an endogenous timing mechanism that integrates endogenous and environmental signalling cues to promote growth. Whereas plants' perception of red and blue portions of the spectrum are well defined, green light sensitivity remains enigmatic. In this study, we show that low fluence rates of green light are sufficient to entrain and maintain circadian rhythms in Arabidopsis and that cryptochromes contribute to this response. Importantly, green light responses are distinguishable from low blue light-induced phenotypes. These data suggest a distinct signalling mechanism enables entrainment of the circadian system in green light-enriched environments, such as those found in undergrowth and in densely planted monoculture.     

Cellular Mechanisms of Entrainment

This review summarizes our current understanding of the signal transduction cascade by which light causes phase shifts of the circadian oscillators found in the eye of Bulla and Aplysia. The isolated retina of these marine mollusks contains a circadian oscillator, a photoreceptor, and a light transduction pathway sufficient for entrainment. This preparation offers unique advantages for the cellular analysis of entrainment and the generation of circadian oscillations. There is evidence that similar cellular mechanisms may underlie mammalian and molluskan circadian oscillations. Thus, the models developed to explain entrainment in the molluskan retina are likely to have utility in exploring the mammalian supra-chiasmatic nucleus.     

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.     

UV-B photoreceptor-mediated signalling in plants

Ultraviolet-B radiation (UV-B) is a key environmental signal that is specifically perceived by plants to promote UV acclimation and survival in sunlight. Whereas the plant photoreceptors for visible light are rather well characterised, the UV-B photoreceptor UVR8 was only recently described at the molecular level. Here, we review the current understanding of the UVR8 photoreceptor-mediated pathway in the context of UV-B perception mechanism, early signalling components and physiological responses. We further outline the commonalities in UV-B and visible light signalling as well as highlight differences between these pathways.     

Melanopsin--shedding light on the elusive circadian photopigment

Circadian photoentrainment is the process by which the brain's internal clock becomes synchronized with the daily external cycle of light and dark. In mammals, this process is mediated exclusively by a novel class of retinal ganglion cells that send axonal projections to the suprachiasmatic nuclei (SCN), the region of the brain that houses the circadian pacemaker. In contrast to their counterparts that mediate image-forming vision, SCN-projecting RGCs are intrinsically sensitive to light, independent of synaptic input from rod and cone photoreceptors. The recent discovery of these photosensitive RGCs has challenged the long-standing dogma of retinal physiology that rod and cone photoreceptors are the only retinal cells that respond directly to light and has explained the perplexing finding that mice lacking rod and cone photoreceptors can still reliably entrain their circadian rhythms to light. These SCN-projecting RGCs selectively express melanopsin, a novel opsin-like protein that has been proposed as a likely candidate for the photopigment in these cells. Research in the past three years has revealed that disruption of the melanopsin gene impairs circadian photo- entrainment, as well as other nonvisual responses to light such as the pupillary light reflex. Until recently, however, there was no direct demonstration that melanopsin formed a functional photopigment capable of catalyzing G-protein activation in a light-dependent manner. Our laboratory has recently succeeded in expressing melanopsin in a heterologous tissue culture system and reconstituting a pigment with the 11-cis-retinal chromophore. In a reconstituted biochemical system, the reconstituted melanopsin was capable of activating transducin, the G-protein of rod photoreceptors, in a light-dependent manner. The absorbance spectrum of this heterologously expressed melanopsin, however, does not match that predicted by previous behavioral and electophysiological studies. Although melanopsin is clearly the leading candidate for the elusive photopigment of the circadian system, further research is needed to resolve the mystery posed by its absorbance spectrum and to fully elucidate its role in circadian photoentrainment.     

Cellular Mechanisms of Entrainment

This review summarizes our current understanding of the signal transduction cascade by which light causes phase shifts of the circadian oscillators found in the eye of Bulla and Aplysia. The isolated retina of these marine mollusks contains a circadian oscillator, a photoreceptor, and a light transduction pathway sufficient for entrainment. This preparation offers unique advantages for the cellular analysis of entrainment and the generation of circadian oscillations. There is evidence that similar cellular mechanisms may underlie mammalian and molluskan circadian oscillations. Thus, the models developed to explain entrainment in the molluskan retina are likely to have utility in exploring the mammalian supra-chiasmatic nucleus.