Photoperiodic Time Measurement Research Articles

Bacteria can anticipate the seasons: photoperiodism in cyanobacteria.

Photoperiodic Time Measurement is the ability of plants and animals to measure differences in day/night-length (photoperiod) and use that information to anticipate critical seasonal transformations such as annual temperature cycles. This timekeeping phenomenon triggers adaptive responses in higher organisms such as gonadal growth/regression, flowering, and hibernation. Unexpectedly, we discovered this capability in cyanobacteria, unicellular prokaryotes with generation times of only 5-6 h. Cyanobacteria in short winter-like days develop enhanced resistance to cold that involves desaturation of membrane lipids and differential programs of gene transcription, including stress response pathways. As in eukaryotes, this photoperiodic timekeeping requires an intact circadian clockwork and develops over multiple cycles. Therefore, photoperiodic timekeeping evolved in much simpler organisms than previously appreciated, and involved genetic responses to stresses that recur seasonally.

Characterization of pre-diapause phase in the northern Drosophila species D. ezoana.

Drosophila ezoana is a virilis group Drosophila species inhabiting northern latitudes. The flies enter adult reproductive diapause to survive winter upon exposure to short photoperiod conditions (short-day) over several consecutive days. Insect pre-diapause phase - the duration between the beginning of exposure to short days and expression of diapause is thought to be comprised of two distinct phases - (a) photoperiodic time measurement that detects short-days, followed by (b) physiological events leading to the expression of diapause phenotype. A short-day dependent segment of the pre-diapause phase thus approximates the process of photoperiodic time measurement. Continuous darkness has been found to be a neutral condition with respect to diapause regulation in many insect species. The effect of variable number of short-days followed by continuous darkness on diapause incidence thus allows identification of short-day dependent segment of pre-diapause phase thereby mapping the process of photo-periodic time measurement. Although, few weeks of exposure to short-days in adult stage is known to be sufficient for the expression of diapause in D. ezoana, the number of short days required for the completion of photo-periodic time measurement has never been systematically analysed. Our experiments show that continuous darkness is a neutral condition for diapause regulation also in D. ezoana. We utilized the neutral nature of continuous darkness to map the process of photoperiodic time measurement in the D. ezoana strain 124OJ8 which showed that integration of short-day photic cues over the first 10 days of pre-diapause phase is essential for diapause induction.

Influence of temperature on the photoperiodic time measurement and on the maternal induction of diapause in Trichogramma telengai: the separation of the two effects

Thermal effects on photoperiodic time measurement and accumulation of inductive photoperiods have been studied in many insect species whereas the influence of temperature on the last step of the photoperiodic response, the induction of diapause, received less attention from researchers. We investigated thermal modification of the maternal photoperiodic response in Trichogramma telengai (Hymenoptera: Trichogrammatidae). Even a single long-night photoperiod experienced by females of this minute egg parasitoid immediately before oviposition causes a substantial increase in larval diapause incidence in the progeny. This feature allows separation of the thermal effects on different steps of the diapause-inducing photoperiodic response. Laboratory experiments showed that the temperature of the last scotophase (when the final decisive photoperiodic time measurement occurs) caused an inverted U-shaped diapause-inducing response similar to that observed in some other long-day insects. The temperature of the last photophase (when progeny diapause is induced) had a positive linear effect that has not been reported for the induction of winter diapause in any long-day insect. Most probably, such a thermal response is not a specific seasonal adaptation but a direct consequence of the influence of temperature on the rate of metabolism.

FSHβ links photoperiodic signaling to seasonal reproduction in Japanese quail

Annual cycles in daylength provide an initial predictive environmental cue that plants and animals use to time seasonal biology. Seasonal changes in photoperiodic information acts to entrain endogenous programs in physiology to optimize an animal’s fitness. Attempts to identify the neural and molecular substrates of photoperiodic time measurement in birds have, to date, focused on blunt changes in light exposure during a restricted period of photoinducibility. The objectives of these studies were first to characterize a molecular seasonal clock in Japanese quail and second, to identify the key transcripts involved in endogenously generated interval timing that underlies photosensitivity in birds. We hypothesized that the mediobasal hypothalamus (MBH) provides the neuroendocrine control of photoperiod-induced changes in reproductive physiology, and that the pars distalis of the pituitary gland contains an endogenous internal timer for the short photoperiod-dependent development of reproductive photosensitivity. Here, we report distinct seasonal waveforms of transcript expression in the MBH, and pituitary gland and discovered the patterns were not synchronized across tissues. Follicle-stimulating hormone-β (FSHβ) expression increased during the simulated spring equinox, prior to photoinduced increases in prolactin, thyrotropin-stimulating hormone-β, and testicular growth. Diurnal analyses of transcript expression showed sustained elevated levels of FSHβ under conditions of the spring equinox, compared to autumnal equinox, short (<12L) and long (>12L) photoperiods. FSHβ expression increased in quail held in non-stimulatory short photoperiod, indicative of the initiation of an endogenously programmed interval timer. These data identify that FSHβ establishes a state of photosensitivity for the external coincidence timing of seasonal physiology. The independent regulation of FSHβ expression provides an alternative pathway through which other supplementary environmental cues, such as temperature, can fine tune seasonal reproductive maturation and involution.

FSHβ links photoperiodic signaling to seasonal reproduction in Japanese quail.

Annual cycles in daylength provide an initial predictive environmental cue that plants and animals use to time seasonal biology. Seasonal changes in photoperiodic information acts to entrain endogenous programs in physiology to optimize an animal's fitness. Attempts to identify the neural and molecular substrates of photoperiodic time measurement in birds have, to date, focused on blunt changes in light exposure during a restricted period of photoinducibility. The objectives of these studies were first to characterize a molecular seasonal clock in Japanese quail and second, to identify the key transcripts involved in endogenously generated interval timing that underlies photosensitivity in birds. We hypothesized that the mediobasal hypothalamus (MBH) provides the neuroendocrine control of photoperiod-induced changes in reproductive physiology, and that the pars distalis of the pituitary gland contains an endogenous internal timer for the short photoperiod-dependent development of reproductive photosensitivity. Here, we report distinct seasonal waveforms of transcript expression in the MBH, and pituitary gland and discovered the patterns were not synchronized across tissues. Follicle-stimulating hormone-β (FSHβ) expression increased during the simulated spring equinox, prior to photoinduced increases in prolactin, thyrotropin-stimulating hormone-β, and testicular growth. Diurnal analyses of transcript expression showed sustained elevated levels of FSHβ under conditions of the spring equinox, compared to autumnal equinox, short (<12L) and long (>12L) photoperiods. FSHβ expression increased in quail held in non-stimulatory short photoperiod, indicative of the initiation of an endogenously programmed interval timer. These data identify that FSHβ establishes a state of photosensitivity for the external coincidence timing of seasonal physiology. The independent regulation of FSHβ expression provides an alternative pathway through which other supplementary environmental cues, such as temperature, can fine tune seasonal reproductive maturation and involution.

Variation in photoperiod response corresponds to differences in circadian light sensitivity in northern and southern Nasonia vitripennis lines

The circadian clock times physiological and behavioural processes and resets on a daily basis to synchronize with the environment. The involvement of the circadian clock in photoperiodic time measurement synchronising annual rhythms is still under debate and different models have been proposed explaining their integration. Insects overcome unfavourable conditions in diapause, a form of dormancy. A latitudinal cline in diapause induction in the parasitoid wasp Nasonia vitripennis as well as a difference in circadian light sensitivity between north and south provide us with additional evidence that the circadian system of Nasonia is involved in photoperiodic time measurement and that latitude-specific seasonality drives adaptive evolution in photoperiodism partly through adaptation responses in the circadian system. We tested diapause induction in a range of T-cycles and photoperiods and found diapause induction in short photoperiods in all T-cycles in the northern line but in the southern line, diapause only occurred in T-cycles close to 24 h. Due to a lower light sensitivity in the southern line, a wider distribution of phase angles of entrainment can be expected at a specific T-cycle duration, while the range of entrainment will decrease. Taking these oscillator properties into account, our data can be explained by an external coincidence model involving a single oscillator with a light-sensitive phase that drives annual timing of diapause in Nasonia vitripennis.

A clock for all seasons in the subterranean.

In 1976, Pittendrigh and Daan established a theoretical framework which has coordinated research on circadian clock entrainment and photoperiodism until today. The "wild clocks" approach, which concerns studying wild species in their natural habitats, has served to test their models, add new insights, and open new directions of research. Here, we review an integrated laboratory, field and modeling work conducted with subterranean rodents (Ctenomys sp.) living under an extreme pattern of natural daily light exposure. Tracking animal movement and light exposure with biologgers across seasons and performing laboratory experiments on running-wheel cages, we uncovered the mechanisms of day/night entrainment of the clock and of photoperiodic time measurement in this subterranean organism. We confirmed most of the features of Pittendrigh and Daan's models but highlighted the importance of integrating them with ecophysiological techniques, methodologies, and theories to get a full picture of the clock in the wild. This integration is essential to fully establish the importance of the temporal dimension in ecological studies and tackling relevant questions such as the role of the clock for all seasons in a changing planet.

Time measurement in insect photoperiodism: external and internal coincidence

The identity and nature of the photoperiodic photoreceptors are now quite well known, as is the nature of the endocrine regulation of the resulting diapauses. The central problem of time measurement—how the photoperiodic clock differentiates long from short days—however, is still obscure, known only from whole-animal experiments and abstract models, although it is clearly a function of the insect circadian system. This review describes some of these experiments in terms of oscillator entrainment and two widely applicable photoperiodic clock models, external and internal coincidence, mainly using data from experiments on flesh flies (Sarcophaga spp) and the parasitic wasp, Nasonia vitripennis.

Impact of photoperiod and functional clock on male diapause in cryptochrome and pdf mutants in the linden bug Pyrrhocoris apterus.

Numerous insect species living in temperate regions survive adverse conditions, such as winter, in a state of developmental arrest. The most reliable cue for anticipating seasonal changes is the day-to-night ratio, the photoperiod. The molecular mechanism of the photoperiodic timer in insects is mostly unclear. Multiple pieces of evidence suggest the involvement of circadian clock genes, however, their role might be independent of their well-established role in the daily oscillation of the circadian clock. Furthermore, reproductive diapause is preferentially studied in females, whereas males are usually used for circadian clock research. Given the idiosyncrasies of male and female physiology, we decided to test male reproductive diapause in a strongly photoperiodic species, the linden bug Pyrrhocoris apterus. The data indicate that reproduction is not under circadian control, whereas the photoperiod strongly determines males' mating capacity. Clock mutants in pigment dispersing factor and cryptochrome-m genes are reproductive even in short photoperiod. Thus, we provide additional evidence of the participation of circadian clock genes in the photoperiodic time measurement in insects.

Hatching rhythm and clock gene expression in the egg of the pea aphid, Acyrthosiphon pisum

Many insects exhibit diel rhythms in physiology and behavior, driven by an endogenous circadian clock. Although aphids are paradigmatic insects whose photoperiodic time measurement is based on a heavily damped circadian clock, there is a lack of empirical data on such a damped circadian clock. The present study investigated the temporal distribution of hatching and the temporal expression patterns of circadian clock genes in the pea aphid, Acyrthosiphon pisum under light–dark (LD) cycles and constant darkness (DD). Hatching occurred intensively in the early photophase, and this rhythm persisted under LD cycles, but damped under DD for a few days. Of the six clock genes analyzed, cyc showed a temporal change in expression under LD cycles, whereas this temporal change was lost under DD. These results suggest that the circadian clock of A. pisum is easily damped during the embryonic stage, supporting the heavily damped oscillator model in photoperiodic time measurement of aphids.

Clock gene-dependent glutamate dynamics in the bean bug brain regulate photoperiodic reproduction.

Animals adequately modulate their physiological status and behavior according to the season. Many animals sense photoperiod for seasonal adaptation, and the circadian clock is suggested to play an essential role in photoperiodic time measurement. However, circadian clock-driven neural signals in the brain that convey photoperiodic information remain unclear. Here, we focused on brain extracellular dynamics of a classical neurotransmitter glutamate, which is widely used for brain neurotransmission, and analyzed its involvement in photoperiodic responses using the bean bug Riptortus pedestris that shows clear photoperiodism in reproduction. Extracellular glutamate levels in the whole brain were significantly higher under short-day conditions, which cause a reproductive diapause, than those under long-day conditions. The photoperiodic change in glutamate levels was clearly abolished by knockdown of the clock gene period. We also demonstrated that genetic modulation of glutamate dynamics by knockdown of glutamate-metabolizing enzyme genes, glutamate oxaloacetate transaminase (got) and glutamine synthetase (gs), attenuated photoperiodic responses in reproduction. Further, we investigated glutamate-mediated photoperiodic modulations at a cellular level, focusing on the pars intercerebralis (PI) neurons that photoperiodically change their neural activity and promote oviposition. Electrophysiological analyses showed that L-Glutamate acts as an inhibitory signal to PI neurons via glutamate-gated chloride channel (GluCl). Additionally, combination of electrophysiology and genetics revealed that knockdown of got, gs, and glucl disrupted cellular photoperiodic responses of the PI neurons, in addition to reproductive phenotypes. Our results reveal that the extracellular glutamate dynamics are photoperiodically regulated depending on the clock gene and play an essential role in the photoperiodic control of reproduction via inhibitory pathways.

Midnight/midday-synchronized expression of cryptochrome genes in the eyes of three teleost species, zebrafish, goldfish, and medaka

Photoperiodic responses are observed in many organisms living in the temperate zones. The circadian clock is involved in photoperiodic time measurement; however, the underlying molecular mechanism for detection of the day length remains unknown. We previously compared the expression profiles of the Cryptochrome(Cry) genes in the zebrafish eye and reported that Cry1ab has a double peak with variable expression duration depending on the photoperiod. In this study, to understand commonalities and differences in the photoperiodic responses of ocular Cry genes, we identified Cryptochrome genes in two other teleost species, goldfish and medaka, living in temperate zones, and measured ocular Cry mRNA levels in all of the three species, under different photoperiods (long-day [14 h light: 10 h dark] and short-day [10 h light: 14 h dark] and in constant darkness. Cry1ab mRNA levels did not show dual peaks in goldfish or medaka under the examined conditions; however, the mRNA expression profiles of many Crys were altered in all three species, depending on the day length and light condition. Based on their expression profiles, Cry mRNA peaks were classified into three groups that better synchronize to sunrise (light-on), midnight/midday (middle points of the dark/light periods), or sunset (light-off). These results suggest the presence of multiple oscillators that oscillate independently or a complex oscillator in which Cry expression cycles change in a photoperiod-dependent manner in the eye.

Photoperiodic regulation of avian physiology: From external coincidence to seasonal reproduction.

Seasonal cycles of environmental cues generate variation in the timing of life-history transition events across taxa. It is through the entrainment of internal, endogenous rhythms of organisms to these external, exogenous rhythms in environment, such as cycling temperature and daylight, by which organisms can regulate and time life history transitions. Here, we review the current understanding of how photoperiod both stimulates and terminates seasonal reproduction in birds. The review describes the role of external coincidence timing, the process by which photoperiod is proposed to stimulate reproductive development. Then, the molecular basis of light detection and the photoperiodic regulation of neuroendocrine timing of seasonal reproduction in birds is presented. Current data indicates that vertebrate ancient opsin is the predominant photoreceptor for light detection by the hypothalamus, compared to neuropsin and rhodopsin. The review then connects light detection to well-characterized hypothalamic and pituitary gland molecules involved in the photoperiodic regulation of reproduction. In birds, Gonadotropin-releasing hormone synthesis and release are controlled by photoperiodic cues via thyrotropin-stimulating hormone-β (TSHβ) independent and dependent pathways, respectively. The review then highlights the role of D-box and E-box binding motifs in the promoter regions of photoperiodic genes, in particular Eyes-absent 3, as the key link between circadian clock function and photoperiodic time measurement. Based on the available evidence, the review proposes that at least two molecular programs form the basis for external coincidence timing in birds: photoperiodic responsiveness by TSHβ pathways and endogenous internal timing by gonadotropin synthesis.

Daylength Shapes Entrainment Patterns to Artificial Photoperiods in a Subterranean Rodent.

Photoperiodism plays an important role in the synchronization of seasonal phenomena in various organisms. In mammals, photoperiod encoding is mediated by differential entrainment of the circadian system. The limits of daily light entrainment and photoperiodic time measurement can be verified in organisms that inhabit extreme photic environments, such as the subterranean. In this experimental study, we evaluated entrainment of circadian wheel-running rhythms in South American subterranean rodents, the Anillaco tuco-tucos (Ctenomys aff. knighti), exposed to different artificial photoperiods, from extremely long to extremely short photophases (LD 21:3, LD 18:6, LD 15:9, LD 9:15, LD 6:18 and LD 3:21). Artificial photoperiods synchronized their activity/rest rhythms and clear differences occurred in (a) phase angles of entrainment relative to the LD cycle and (b) duration of the daily activity phase α. These photoperiod-dependent patterns of entrainment were similar to those reported for epigeous species. Release into constant darkness conditions revealed aftereffects of entrainment to different photoperiods, observed in α but not in the free-running period τ. We also verified if animals coming from summer and winter natural photoperiods entrained equally to the artificial photoperiods by evaluating their phase angle of entrainment, α and τ aftereffects. To this end, experimental animals were divided into "Matching" and "Mismatching" groups, based on whether the experimental photoperiod (short-day [L < 12 h] or long-day [L > 12 h]) matched or not the natural photoperiod to which they had been previously exposed. No significant differences were found in the phase angle of entrainment, α and τ aftereffects in each artificial photoperiod. Our results indicate that the circadian clocks of tuco-tucos are capable of photoperiodic time measurement despite their natural subterranean habits and that the final entrainment patterns achieved by the circadian clock do not depend on the photoperiodic history.

Effects of light pollution on photoperiod-driven seasonality

Changes to photoperiod (day length) occur in anticipation of seasonal environmental changes, altering physiology and behavior to maximize fitness. In order for photoperiod to be useful as a predictive factor of temperature or food availability, day and night must be distinct. The increasing prevalence of exposure to artificial light at night (ALAN) in both field and laboratory settings disrupts photoperiodic time measurement and may block development of appropriate seasonal adaptations. Here, we review the effects of ALAN as a disruptor of photoperiodic time measurement and season-specific adaptations, including reproduction, metabolism, immune function, and thermoregulation.

Time measurement in insect photoperiodism: The role of photophase duration and light intensity

The initial stages of diapause induction - as summer gives way to autumn - involve a process of time measurement in which the duration of daylength (or nightlength) is determined by a photoperiodic 'clock' based upon the circadian system. In many insects so far examined, a photophase of sufficient duration and illuminance resets a photoperiodic oscillator to a constant phase equivalent to the beginning of the 'subjective night' (Circadian time, CT 12 h) whereupon it proceeds to measure nightlength in a clock of the external coincidence type. A possible exception may be found in the linden bug, Pyrrhocoris apterus, which - in laboratory studies using relatively low light intensity - suggests that daylength is measured rather than the night. Earlier studies of photoperiodic responses (pupal diapause induction) in the flesh fly Sarcophaga argyrostoma, however, showed that 'weak' or short light pulses giving rise to Type 1 phase response curves could be converted by increasing light intensity to Type 0 responses that phase set the oscillation to the beginning of the subjective night (CT 12 h) whereupon it could begin to measure the night. Based upon these data it is therefore suggested that the photoperiodic clock in P. apterus might also measure nightlength if the bugs were exposed to photophases of higher irradiance simulating daytime exposure to the light intensity experienced by these diurnally active insects in their natural environment.

The circadian clock gene (Clock) regulates photoperiodic time measurement and its downstream process determining maternal induction of embryonic diapause in a cricket

In response to short days in autumn, most temperate multivoltine insects enter diapause, a state in which development or reproduction is suppressed or arrested, which serves to coordinate their development and physiology (or that of offspring) with annual changes in the environment (i.e. photoperiodism). This response is mediated by a measurement of time based on photoperiod (photoperiodic time measurement), which is thought to be regulated by a circadian clock. However, some studies also demonstrate the involvement of the circadian clock in an output process that generates phenotypes associated with diapause. To gain further insight into this, we silenced the Clock (Clk) gene, the main regulator of the circadian clock, in the band-legged ground cricket Dianemobius nigrofasciatus (Orthoptera: Trigonidiidae). Silencing the Clk gene using RNA interference (Clk RNAi) in female crickets resulted in abnormal circadian rhythms under constant darkness and light-dark conditions, thereby indicating the central role of this gene in the circadian clock mechanism. Clk RNAi females exhibited long-day oviposition behaviour, even when reared under short-day conditions, thereby indicating the involvement of Clk in photoperiodic time measurement. In addition, Clk RNAi females immediately laid non-diapause-type eggs, which was not recorded in control females under either short-day or long-day conditions and cannot be explained in terms of dysfunction of photoperiodic time measurement. Accordingly, we speculate that Clk could also be involved in a downstream process that results in the laying of diapause-type eggs.

Insect photoperiodism: Bunning's hypothesis, the history and development of an idea

In insects, the photoperiodic system comprises a linked sequence of events from photoreception to final seasonally-appropriate phenotypes such as overwintering diapause. The first and last of these events are reasonably well known, but central phenomena such as those distinguishing short from long days (time measurement) and the nature, accumulation and transfer of this information through development, metamorphosis and sometimes across generations remains obscure. BĂźnning's intuitive suggestion that photoperiodic time measurement was a function of the circadian system, made eight decades ago, however, has provided a framework for numerous studies investigating these connections. This review examines the development of BĂźnning's hypothesis from its origin in plants to the physiology of diapause in insects. Despite considerable inter-species differences, a close and probably causal relationship between circadian rhythmicity and photoperiodism is indicated.

Insect photoperiodism: Seasonal development on a revolving planet

This review starts by comparing photoperiodic diapause with non-photoperiodic quiescence in four representative species, paying particular attention to overwintering in Drosophila melanogaster. In the second part it describes dormancy strategies of insects from the equator to the polar regions, addressing topics such as the role of the circadian system in photoperiodic time measurement, latitudinal clines in diapause-related traits, hourglass-like photoperiodic clocks based on dampening circadian oscillators, and the dormancy strategies of insects close to the equator or at high latitudes where seasonal changes in photoperiod are unreliable or absent.

A photoperiodic time measurement served by the biphasic expression of Cryptochrome1ab in the zebrafish eye

The zebrafish (Danio rerio) is a model species that is used to study the circadian clock. It possesses light-entrainable circadian clocks in both central and peripheral tissues, and its core circadian factor cryptochromes (CRYs) have diverged significantly during evolution. In order to elucidate the functional diversity and involvement of CRYs in photoperiodic mechanisms, we investigated the daily expression profiles of six Cry transcripts in central (brain and eye) and peripheral (fin, skin and muscle) tissues. The zCry genes exhibited gene-specific diurnal conserved variations, and were divided into morning and evening groups. Notably, zCry1ab exhibited biphasic expression profiles in the eye, with peaks in the morning and evening. Comparing ocular zCry1ab expression in different photoperiods (18L:6D, 14L:10D, 10L:14D and 6L:18D) revealed that zCry1ab expression duration changed depending on the photoperiod: it increased at midnight and peaked before lights off. zCry1ab expression in constant light or dark after entrainment under long- or short-day conditions suggested that the evening clock and photic input pathway are involved in photoperiod-dependent zCry1ab expression. Laser microdissection followed by qRT-PCR analysis showed that the evening peak of zCry1ab was likely ascribed to visual photoreceptors. These results suggest the presence of an eye-specific photoperiodic time measurement served by zCry1ab.