Journal of Experimental Botany, Vol. 53, No. 374, pp. 1535-1550,
July 1, 2002
© 2002 Oxford University Press
Signs of the time: environmental input to the circadian clock
Received 25 September 2001; Accepted 18 April 2002
Division of life Sciences, King’s College London, Franklin-Wilkins Building, 150 Stamford Street, London SE1 8WA, UK
1 Fax: +44 (0)20 7848 4500. E-mail: paul.devlin{at}kcl.ac.uk
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Abstract |
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 Top Abstract IntroductionLight input to the...Circadian photoperception in...Photoreceptors involved in light...Oscillating photoreceptor...Photoreceptors involved in light...Photoreceptors involved in light...Differences in circadian...Photoreceptors involved in light...Temperature input to the...ConclusionsReferences |
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The circadian clock forms one of the most fascinating adaptations to life on earth. Organisms can not only anticipate the day/night cycle but can make use of an internal clock to measure daylength as an indicator of the changing of the seasons. The innate period of the clock is not exactly equal to 24 h, but is reset each day by environmental signals at dawn and dusk, most notably by changes in light and temperature. This ability to re-entrain also ensures that the clock is synchronized with the day/night cycle which in turn is crucial for anticipation of dawn and dusk. Recent advances in the field have identified the photoreceptors involved in resetting the clock in several systems. This has revealed surprising similarities, but also key differences in the circadian systems of plants, fungi, insects, and mammals. One recurring feature emerging from this research is that the photoreceptors themselves are under the control of the clock with transcript abundance being tightly regulated. Furthermore, elements of a feedback pathway whereby the clock modulates the activity of the light input pathway are now being identified.
Key words: Key words: Circadian clock, environmental input, photoreceptors, temperature.
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Introduction |
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TopAbstractIntroductionLight input to the...Circadian photoperception in...Photoreceptors involved in light...Oscillating photoreceptor...Photoreceptors involved in light...Photoreceptors involved in light...Differences in circadian...Photoreceptors involved in light...Temperature input to the...ConclusionsReferences |
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All organisms properly tested show a rhythm of metabolism, of physiological processes or even of behaviour in tune with the day/night cycle of the earth. In plants, the components of the photosynthetic machinery accumulate each day in anticipation of dawn; leaves or flowers often close up just before dusk to provide protection for more delicate tissues from the lower temperatures of night (Darwin, [1895] 1981; Enright, 1982). In insects, the adult flies eclose from their pupae in synchrony with dawn to provide the maximum chances of survival (Pittendrigh, 1954), in mammals such as ourselves our body has a rhythm of alertness and of temperature that causes us to be active during the day and to sleep at night (Moore-Ede et al., 1982). These phenomena are not purely responses to the external environment and will continue even in the absence of any external cues. A plant maintained in constant light will still show a cyclic production of its photosynthetic machinery (Millar and Kay, 1991), a human deep underground will continue to wake and sleep with an approximately 24 h rhythm as if still experiencing dawn and dusk (Luce, 1971; Sulzman, 1983). Such processes are controlled by an endogenous oscillator known as the circadian clock which continues to cycle, maintaining its own, approximately 24 h rhythm, as a result of the oscillation of the levels or activity of molecules within the cells of each organism. The molecules making up this core clock and their biochemical interactions have been well studied and in insects and mammals the components of this basic ‘clock mechanism’ are now known. These are discussed in more detail by Wager-Smith and Kay (2000). In plants, the clock mechanism remains more elusive, but several recent advances have begun to shed light on this (Carré and King, 2002).
The circadian clock does not run in isolation from the cycle of day and night. It must, itself, be set to the correct time. The clock must include a resetting mechanism by which it can first be synchronized with the day/night cycle so that the organism can correctly anticipate dawn and dusk. This clock resetting is a phenomenon very familiar to any travellers on long-haul flights. When a person travels through several time-zones, initially jet-lag is experienced whereby his/her circadian clock remains set to the timing of dawn and dusk in the place of departure though, gradually, over the course of a few days he/she finds his/her rhythm of sleep and wake has adjusted to the new timing of dawn and dusk.
The two most prevalent environmental cues which act as Zeitgebers (time givers) are the changes in light and temperature occurring at dawn and dusk and both are capable of resetting the clock (Edmunds, 1988; Roenneberg and Foster, 1997). The circadian clock can be thought of in terms of three major components: an ‘input’ pathway by which environmental cues act to synchronize the clock; the endogenous ‘oscillator’ itself; and the ‘output’ pathway whereby the rhythmic metabolic systems controlled by the clock are co-ordinated (Fig. 1). This review focuses on the input to the clock. More details on clock output can be found in three recent papers by Harmer et al. (2000), McDonald et al. (2001) and Duffield et al. (2002), focusing on plants, insects and mammals, respectively. However, one caveat should be added to this separation in that it is now apparent that this traditional three component model of the circadian system is over-simplistic and it is becoming increasingly more difficult to consider any one of these components in isolation. For example, it has been clear for some time that the output pathway modulates (gates) the sensitivity of the input pathway (Fig. 1). Consequently, this review takes a fairly holistic approach in describing the input pathway.
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Light input to the circadian clock |
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TopAbstractIntroductionLight input to the...Circadian photoperception in...Photoreceptors involved in light...Oscillating photoreceptor...Photoreceptors involved in light...Photoreceptors involved in light...Differences in circadian...Photoreceptors involved in light...Temperature input to the...ConclusionsReferences |
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Light forms the dominant signal in resetting the clock and a close link between the circadian photoreceptors and the clock itself has been demonstrated for several systems (Devlin and Kay, 2001). In fact, the distinction between input, oscillator and output is becoming more and more blurred as more is discovered about the mechanism itself.
In resetting, the clock exhibits a change in phase. That is, the hands of the circadian clock are moved forward or backwards. In terms of the molecular mechanism of the clock this would represent a change in the level or activity of a clock component to a level or activity that would normally be found at a different point in the cycle (Crosthwaite et al., 1995). The clock then continues as before. For most organisms the period of the circadian cycle is not quite 24 h and they show a slight resetting with each dawn and/or dusk. This plasticity allows an organism to adjust continually to changing daylength as the seasons of the year progress. The response of the clock to light is different at different times of day. The onset of light prior to the expected dawn will generally cause an advance in the phase of the rhythm whilst extension of the light period after the expected dusk will generally cause a delay in the phase of the rhythm. It is possible to produce a ‘phase response curve’ (PRC) illustrating this effect (Johnson, 1990). The effects of light pulses at different times of day on the phase of the rhythm are examined for organisms otherwise maintained in darkness. An example of a typical phase response curve is shown in Fig. 2. The curve shows a strong phase-advance response around subjective dawn and a strong phase-delay response around subjective dusk. The response to light is greatly reduced during the subjective day, as might be expected, when the organism will normally be ‘seeing’ light. For many organisms the PRC exhibits a ‘dead-zone’ during the subjective day where no response at all is seen to light (Johnson, 1990).
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Entrainment of the circadian clock by such pulses of light is known as non-parametric entrainment as opposed to parametric entrainment to day/night cycles. Although the clock is sensitive to pulses of light for resetting, it is important that the clock should not be unduly influenced by aberrations in the environment. It must not, for example, be reset by a flash of lightning at night. In general, a prolonged pulse of irradiation is required to reset the clock (Nelson and Takahashi, 1991).
The photoreceptors involved in the perception of light leading to resetting of the circadian clock have been the subject of several recent advances in the field of circadian biology. Both plants and animals have a complex array of photoreceptors (Roenneberg and Foster, 1997; Whitelam and Devlin, 1998; Foster, 1998; Hall, 2000). The photoreceptors in plants are particularly well characterized. Light plays a key role in the development of a plant, controlling processes from germination, through seedling establishment, to determining the whole architecture of the plant (Kendrick and Kronenberg, 1994). Plants are exquisitely sensitive to small changes in the light environment in order to be able to adapt to take maximum advantage of the available light for photosynthesis. The first identification of the photoreceptors involved in resetting of the circadian clock came from research in the model plant, Arabidopsis thaliana where two families of photoreceptors, the red-absorbing phytochromes and the blue-absorbing cryptochromes combine to relay dawn and dusk signals to the endogenous oscillator (Somers et al., 1998a). In insects and mammals, the blue light photoreceptor, cryptochrome was also discovered and demonstrated to play a key role in the circadian clock. In insects, cryptochrome is the main circadian photoreceptor although it has also been proposed to play a role in the oscillator mechanism in peripheral tissue (Emery et al., 1998, 2000; Stanewsky et al., 1998; Krishnan et al., 2001). In mammals, the main role of cryptochrome is as a component of the central clock mechanism itself (Kume et al., 1999; (van der Horst et al., 1999). The photoreceptors involved in the perception of light in resetting the clock remain elusive. It is known, however, that the eyes are essential for entrainment in mammals (Foster, 1998) yet several pieces of research have ruled out the involvement of the visual opsins (Freedman et al., 1999).
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Circadian photoperception in plants |
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TopAbstractIntroductionLight input to the...Circadian photoperception in...Photoreceptors involved in light...Oscillating photoreceptor...Photoreceptors involved in light...Photoreceptors involved in light...Differences in circadian...Photoreceptors involved in light...Temperature input to the...ConclusionsReferences |
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The earliest recorded observation of a circadian rhythm was made by Androsthenes (historian of Alexander the Great) around 400 bc. He observed that leaves of several tree species exhibit a horizontal position during the day and a more vertical position at night. However, it was in 1729 that the French astronomer, Jean Jacques d’Ortous de Mairan first demonstrated that this was the result of the action of an endogenous circadian clock. Mimosa, the sensitive plant, folds up its leaves at night and opens them again in the day. De Mairan showed that this rhythm, continued even when the plants were placed in deep shade demonstrating that bright sunlight was not required to trigger this response (de Mairan, 1729).
In plants, a large range of physiological processes are controlled by the circadian clock including rhythmic leaf movements (Engelmann et al., 1994; Millar et al., 1995a), photoperiodic induction of flowering (Devlin and Kay, 2000b) and stomatal opening (Somers et al., 1998b). However, much of the work studying the circadian clock in plants has involved the analysis of the rhythm of expression of the clock-controlled gene, light-harvesting chlorophyll a/b protein (better known as the chlorophyll a/b binding protein, CAB). CAB forms part of the photosynthetic machinery of the plant and, as would be predicted, the CAB transcript begins to accumulate prior to dawn, shows a peak of expression in the early part of the day then decreases again towards dusk (Millar and Kay, 1991). Millar et al. (1992) attached a firefly luciferase reporter gene (LUC) to the CAB promoter and transformed this CAB::LUC construct into plants. Using a highly sensitive photon-counting camera they were able to follow the rhythmic expression pattern of CAB in living seedlings by following the transient bioluminescence of the firefly luciferase produced as a result (Fig. 3).
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This system allowed the isolation of several circadian clock mutants in A. thaliana (Millar et al., 1995a). One of these was the result of a mutation in the gene, TIMING OF CAB 1 (TOC1), that encodes a pseudo-response regulator involved in the central clock mechanism in A. thaliana (Strayer et al., 2000). The toc1 mutation affects all known observable rhythms in A. thaliana even in constant darkness and the TOC1 message, itself, displays circadian oscillation with a peak at subjective dusk, thus demonstrating its credentials as a central clock component (Somers et al., 1998a, b; Strayer et al., 2000). Other methods looking at the transcription factors responsible for regulation of the CAB gene identified two other central clock components, LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), both MYB-type transcription factors (Wang and Tobin, 1998; Schaffer et al., 1998). Mutations in cca1 and lhy, likewise affect all known observable rhythms in A. thaliana and the CCA1 and LHY transcripts oscillate with a circadian rhythm showing a peak of expression at subjective dawn (Wang and Tobin, 1998; Schaffer et al., 1998). It was recently demonstrated that TOC1 is responsible for the positive regulation of CCA1 and LHY expression, whilst both LHY and CCA1 bind to the TOC1 promoter for the negative regulation of TOC1 expression (Alabadi et al., 2001). This loop (represented in the ‘Oscillator’ section of Fig. 4) is critical for clock function in A. thaliana and is proposed to form the fundamentals of the central circadian oscillator in A. thaliana.
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The CAB::LUC reporter system was also used to analyse the light input pathway to the plant circadian clock. Millar et al. (1995b) demonstrated that the A. thaliana circadian clock ran faster in continuous light than in darkness. The response of an endogenous oscillator to continuous light is the sum of the phase advances and phase delays occurring throughout the circadian cycle. As light intensity increases, the magnitude of these phase shifts increases (Aschoff, 1979). The overall effect depends on the shape of the phase response curve. In diurnal organisms, such as A. thaliana, phase advances predominate over phase delays with the result that, in continuous light, increasing light intensity tends to lead to a shortening of the circadian period length. In nocturnal organisms, phase delays predominate over phase advances with the result that increasing light intensity tends to lead to a lengthening of period length. This phenomenon has become known as Aschoff’s rule (Aschoff, 1979). Millar et al. (1995b) showed that both red and blue light were capable of causing a shortening of the CAB::LUC rhythm in A. thaliana.
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Photoreceptors involved in light input to the circadian clock in plants |
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TopAbstractIntroductionLight input to the...Circadian photoperception in...Photoreceptors involved in light...Oscillating photoreceptor...Photoreceptors involved in light...Photoreceptors involved in light...Differences in circadian...Photoreceptors involved in light...Temperature input to the...ConclusionsReferences |
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In addition to chlorophyll, which carries out light harvesting for photosynthesis, plants possess several information gathering photoreceptors that allow them to regulate their development to take maximum advantage of their light environment. These fall into three families, the phytochromes, absorbing red and far red light and the cryptochromes and the phototropins, absorbing blue and UV wavelengths (Whitelam and Devlin, 1998; Christie and Briggs, 2001). The phytochrome family consists of five members in A. thaliana, phyA to phyE (Sharrock and Quail, 1989; Clack et al., 1994). All share the same basic structure, comprising a protein moiety of about 124 kDa and a covalently attached linear tetrapyrrole chromophore (Quail, 1991). Phytochromes exist in two photo-interconvertible forms, a red-absorbing, Pr form and a far-red-absorbing Pfr form (Quail, 1991). Phytochrome is synthesized in the inactive Pr form and upon absorption of a photon of light is converted to the active Pfr form that is responsible for regulating a range of physiological and developmental responses. PhyA is light labile and accumulates to high levels in etiolated seedlings (Quail, 1991). PhyA acts most prominently in germination and in seedling establishment and triggers a response to very low levels of light (Whitelam et al., 1993; Johnson et al., 1994). It is rapidly degraded in high fluences of red light and hence phyA is thought of as an ‘antenna’ detecting the small amount of light penetrating through the upper layer of soil indicating that a seedling is about to emerge into light (Yanovsky et al., 1995). PhyB–phyE are light stable and are generally involved in responses to higher fluences of red light (Hirschfeld et al., 1998; Whitelam et al., 1998). It is noticeable that the phytochromes also show a peak of absorption in the blue region of the spectrum and, consistent with this, phytochrome A has been implicated in some blue light responses (Whitelam et al., 1993). Sufficient phyA Pfr is formed in blue light to trigger a response.
The cryptochrome family in A. thaliana comprises two members, cry1 and cry2 (Devlin and Kay, 1999). Cryptochromes show a strong resemblance to the photolyases involved in the blue/UV light-dependent repair of DNA damage (Cashmore et al., 1999). The N-terminal section of each of the A. thaliana cryptochromes shares a strong homology with type II photolyase and, like the photolyases, cryptochromes bind two chromophores, a light-harvesting pterin and a catalytic flavin (Malhotra et al., 1995; Lin et al., 1995). Cry1 is light stable whilst cry2 is light labile and is degraded under high fluences of blue light (Lin et al., 1998). Cry2 has been demonstrated to be involved in seedling establishment in low fluence blue light whilst cry1 shows an involvement in such responses at both low and high fluences of blue (Lin et al., 1998).
Somers et al. (1998a) demonstrated that both phytochromes and cryptochromes contribute to light input to the circadian clock in A. thaliana. By crossing the CAB::LUC transgene into null mutants for phyA, phyB, cry1 or cry2, roles for phyA and cry1 in the perception of blue light, and phyA and phyB in the perception of red light were demonstrated (Somers et al., 1998a). The assay made use of Aschoff’s rule whereby increasing fluence rate (light intensity) causes a decreasing period length in constant light (Aschoff, 1979). PhyA mutant seedlings showed a deficiency in the perception of low fluence rates of red and blue light consistent with the role of phyA as a low fluence photoreceptor in seedling establishment. PhyB mutant seedlings showed a deficiency in the perception of high fluence rate red light (Somers et al., 1998a). The responses of the phyA and phyB mutant seedlings nicely demonstrates the plasticity of recruitment of photoreceptors by the plant to allow meaningful detection of a range of fluence rates. Red light fluence rates above which the phyA response would saturate fall within the active range of phyB. At these fluence rates, phyA is degraded and phyB becomes the dominant red light photoreceptor. Studies with phyA phyB double mutants confirm these findings showing an additivity between the phyA and phyB monogenic phenotypes (Devlin and Kay, 2000a).
Cry1 mutants showed a deficiency in response to low fluence rates of blue light, a wild-type response to intermediate fluence rates of blue light and a deficiency in response to high fluence rates of blue light. This clearly indicated a role for cry1 in blue light input to the clock. The cry2 monogenic mutant showed a wild-type response for blue light input to the clock (Somers et al., 1998a), but analysis of the cry1 cry2 double mutant showed a redundancy between cry1 and cry2 at intermediate fluence rates (Devlin and Kay, 2000a). This is consistent with the way in which cry1 and cry2 act in seedling establishment at these fluence rates. Both cry1 and cry2 act in seedling establishment in lower fluence rates of blue light, but cry2 is degraded at higher fluence rates leaving cry1 as the sole blue light photoreceptor for de-etiolation (Lin et al., 1998).
Significantly, for light input to the clock the cry1 mutant was also found to show a deficiency in the perception of low fluence rate red light in a similar manner to that seen in the phyA mutant (Devlin and Kay, 2000a). Given the fact that the absorption spectrum for the cryptochromes shows no peak in the red region of the spectrum, it must be concluded that cryptochrome is acting downstream of the photoreceptor phyA, presumably as a signal transduction component. Double mutant analysis of phyA cry1 in white light confirms that there is no additivity between these two mutations for low fluence rate light input to the clock (Devlin and Kay, 2000a). Both phyA and cry1 are capable of acting as photoreceptors in white light, yet cry1 is epistatic to phyA. This suggests that in low fluence rates of both red and blue light cry1 acts purely as a signal transduction component downstream of phyA. This role for cry1 appears unique to circadian photoperception. No evidence was found for a role for cry1 in seedling de-etiolation in low fluence rates of red light (Devlin and Kay, 2000a). A scheme for the action of the cryptochromes in blue light input to the clock is shown in Fig. 5a.
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Evidence for the action of phyD and phyE in red light input to the clock was also demonstrated. In the regulation of physiological development in A. thaliana phyD and phyE show a conditional redundancy with phyB in that the roles of phyD and phyE only become apparent in the absence of phyB (Whitelam et al., 1998). This also appears to be the case for the action of phyD and phyE in light input to the clock. The phyD and phyE monogenic mutants show a wild-type response to red light, but when the phyA phyB phyD triple mutant was compared to the phyA phyB double mutant, the phyA phyB phyD triple mutant showed a relative deficiency in the perception of high fluence rate red light. Likewise the phyA phyB phyE triple mutant showed a deficiency in the perception of high fluence rate red light relative to the phyA phyB double mutant (Devlin and Kay, 2000a). The redundancy between phyD or phyE and phyB is, to some extent, understandable, given the fairly close similarity between the DNA sequences of phyB, phyD and phyE. In particular, phyB and phyD of A. thaliana are thought to have arisen as the result of a very recent gene duplication subsequent to the divergence of the Cruciferae and the Solanaceae (Mathews and Sharrock, 1997). Significantly the phyA phyB phyD triple mutant and the phyA phyB phyE triple mutant both still showed a significant shortening of period length as red light fluence rate increased, indicating, in each case, the action of the remaining phytochromes in red light input to the clock (Devlin and Kay, 2000a). Whether this represents the action of phyC awaits the creation of the phyA phyB phyD phyE quadruple mutant. One important point to note is that the photoreceptor mutants show no effect on the period length of the clock in darkness indicating that they are purely affecting the light input pathway rather than disrupting the clock mechanism itself (Devlin and Kay, 2000a). The roles of the phytochromes and the cryptochromes in light input to the circadian clock can be summarized as in Fig. 4b.
The third class of plant photoreceptors, the phototropins, are involved in the perception of blue wavelengths of light, leading to phototropism (Huala et al., 1998; Jarillo et al., 1998; Kagawa et al., 2001). Two phototropins are present in A. thaliana, nph1 (named after the mutant phenotype, non-phototropic hypocotyl) (Liscum and Briggs, 1995) and npl1 (nph1-like) (Kagawa et al., 2001). Phototropins consist of a protein moiety with two flavin chromophores held within PAS or LOV domains within the protein molecule (Christie et al., 1998). Analysis of the response of the nph1 mutant to a range of fluence rates of blue light showed no evidence for the involvement of nph1 in light input to the clock (Harmer et al., 2000; supplemental data), however, it remains possible that nph1 could act redundantly with other photoreceptors.
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Oscillating photoreceptor expression |
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TopAbstractIntroductionLight input to the...Circadian photoperception in...Photoreceptors involved in light...Oscillating photoreceptor...Photoreceptors involved in light...Photoreceptors involved in light...Differences in circadian...Photoreceptors involved in light...Temperature input to the...ConclusionsReferences |
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In several systems, a close association between light input and the clock itself has been established with the result that the traditional distinction of input, oscillator and output is becoming blurred. Transcription of the PHYB gene and of the CRY1 and CRY2 genes in A. thaliana was recently shown to oscillate with a circadian rhythm in continuous light (Bognar et al., 1999; Harmer et al., 2000). PHYB shows a peak around subjective dawn whilst the CRYs show a peak in the later part of the subjective day (Harmer et al., 2000). The circadian photoreceptors, phyB, cry1 and cry2 are therefore part of both the input and output pathways from the clock and in this way the output pathway may feed back on the input pathway, adding an additional level of fine tuning to the clock resetting mechanism (Fig. 4). It is possible that the expression pattern of the circadian photoreceptors may, to some extent, contribute to the shape of the phase response curve giving increased sensitivity to light at the dawn and dusk transitions.
Such modulation of light responsiveness over the course of the circadian cycle has been termed gating (Millar and Kay, 1996). Gating is not only observed for clock resetting but also for several clock outputs which can also be directly regulated by light. Control of CAB gene expression is directly light responsive as well as being clock regulated. Following a period of darkness, CAB gene expression will show an acute spike in transcription in response to a light pulse. However, a strong circadian rhythm in this light responsiveness of CAB induction is observed, indicating that light-signalling to CAB is strongly gated by the clock (Millar and Kay, 1996). Very recently, the first candidate for a protein involved in this gating process was identified in A. thaliana. The elf3 mutant shows an arrhythmic phenotype in constant white light (Hicks et al., 1996) but does show a circadian rhythm in darkness. McWatters et al. (2000) demonstrated that the elf3 mutant fails to show any gating of the acute response of CAB in darkness. They concluded that the arrest of the oscillator in constant light is also a result of a loss of gating of light input, demonstrating that gating of phototransduction is an important part of the resetting response (McWatters et al., 2000) (Fig. 4).
Candidates for factors involved in the light input pathway downstream of the photoreceptors themselves have also been identified in plants. The zeitlupe (ztl) mutant of A. thaliana was identified as showing a long period length for the rhythm of CAB::LUC expression in constant light (Somers et al., 2000). It also shows a long period length for expression of other circadian clock regulated genes and for the rhythm of cotyledon movement (Somers et al., 2000). The ztl phenotype is strongly dependent on fluence rate, displaying a greater period lengthening effect at lower fluence rates (Somers et al., 2000). This suggests that ztl specifically disrupts light input to the clock. ZTL forms part of a small family of three closely related proteins along with FKF1 and LKP2 (Nelson et al., 2000; Kiyosue and Wada, 2000). FKF1 also affects circadian regulated gene expression and mutations in both ZTL and FKF1 both cause late flowering (Somers et al., 2000; Nelson et al., 2000). Recently ZTL was demonstrated to bind to both phyB and cry1 using yeast two-hybrid and in vitro binding studies, further suggesting a close association with the light input pathway to the circadian clock (Jarillo et al., 2001) (Fig. 4).
Another candidate signal transduction component downstream of phytochrome in light input to the clock is PHYTOCHROME INTERACTING FACTOR 3 (PIF3). PIF3 was identified in a yeast two-hybrid screen for phytochrome interacting factors (Ni et al., 1998). The PIF3 gene encodes a bHLH-type transcription factor that binds to G-box sequences present in the promoters of the genes encoding the critical clock components, LHY and CCA1 (Martinez-Garcia et al., 2000). When a phytochrome molecule is converted to the Pfr form it moves from the cytoplasm to the nucleus and there binds to the promoter-bound PIF3 transcription factor (Kircher et al., 1999; Ni et al., 1999). CCA1 and LHY gene expression is light-regulated and PIF3 has been shown to be essential for normal light regulation (Ni et al., 1999). This has led to the conclusion that binding of phytochrome to PIF3 acts as the switch to trigger an increase in expression of the CCA1 and LHY genes. Such a system would allow a pulse of light to reset the clock by triggering a change in CCA1 and LHY message levels (Fig. 4).
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Photoreceptors involved in light input to the circadian clock in insects |
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TopAbstractIntroductionLight input to the...Circadian photoperception in...Photoreceptors involved in light...Oscillating photoreceptor...Photoreceptors involved in light...Photoreceptors involved in light...Differences in circadian...Photoreceptors involved in light...Temperature input to the...ConclusionsReferences |
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Following the discovery of cryptochromes in plants (Ahmad and Cashmore, 1993), molecules showing strong similarity to photolyases, but which failed to show any photolyase function, were identified in animals (Sancar, 2000). Because of this similarity to the plant cryptochromes, these molecules were also termed cryptochromes. As with the plant cryptochromes, the N-terminus of the animal cryptochromes shows strong homology to the photolyases whilst the C-terminal forms a unique extension (Cashmore et al., 1999; Devlin and Kay, 1999; Sancar, 2000). However, the animal cryptochromes show a stronger homology with the 6-4 photolyases than with the type II photolyases (Cashmore et al., 1999). It is thought that the animal cryptochromes arose subsequent to the plant cryptochromes by divergence from the 6-4 photolyases. The phylogeny of the plant cryptochromes, however, suggests that they arose much earlier. In fact, they are predicted to have arisen prior to the divergence of plants and animals (Cashmore et al., 1999) suggesting that plant-like, type II photolyase-derived cryptochrome has been subsequently lost in animals. None-the-less, the same blue-light-sensing mechanism seems to have been adapted once again to provide a circadian photoreceptor in animals, particularly in insects where cryptochrome forms the primary circadian photoreceptor (Emery et al., 2000; Devlin and Kay, 2001). The core clock components have been well characterized in the insect, Drosophila melanogaster, where a transcriptional feedback loop involving four key molecules generates sustained oscillation at the molecular level with a relatively tight circadian period (Allada et al., 1998; Rutila et al., 1998; Darlington et al., 1998). Transcription of the genes, period (per) and timeless (tim) leads to a rise in PER and TIM protein levels in the afternoon and early evening. PER–TIM dimers then enter the nucleus and repress their own transcription by inhibiting the activity of a positively acting transcriptional activation complex consisting of the proteins CLOCK (CLK) and CYCLE (CYC). Consequently, levels of PER and TIM protein fall again as these proteins are degraded until they reach a level at which they no longer inhibit their own transcription and the cycle begins again (Allada et al., 1998; Rutila et al., 1998; Darlington et al., 1998) (Fig. 6).
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A second, interlocked negative feedback loop causes CLK to cycle in antiphase with PER and TIM. In this, CLK feeds back as a repressor of its own transcription whilst PER and TIM act as derepressors (Glossop et al., 1999).
In D. melanogaster it was known that visual photoreceptors alone were not responsible for light input to the clock. The norpAp41 mutation causes the compound eyes and ocelli to be completely unresponsive to light, although monogenic norpAp41 mutant flies show normal entrainment (Wheeler et al., 1993; Yang et al., 1998). The discovery of cryptochrome provided a strong candidate for the circadian photoreceptor. A D. melanogaster mutant lacking cryptochrome, named crybaby (cryb) has been most informative in revealing the role of cryptochrome in the D. melanogaster clock. In the cryb mutant, rhythms of PER and TIM expression in the body of the fly fail to entrain to light/dark cycles (Stanewsky et al., 1998). Curiously, cryb mutant flies were still observed to display behavioural locomotor rhythms. It was subsequently discovered that the rhythm of per and tim expression within lateral neuron cells remains entrainable by light suggesting that photoreceptors other than D. melanogaster cryptochrome (dCRY) are able to entrain these rhythms. When the norpAp41 mutation was combined with the cryb mutation, norpAp41 cryb double mutant flies now failed to show normal entrainment of behavioural rhythms (Stanewsky et al., 1998) suggesting that behavioural entrainment in D. melanogaster is mediated by a combination of signals from cryptochrome and from the visual photoperception pathway.
Phase shifting is also compromized in the cryb mutant flies. In response to a pulse of light that will induce a phase shift in behavioural rhythms in wild-type flies, the cryb mutant fails to show any phase shift (Stanewsky et al., 1998). Responses of overexpressors of dcry, however, vary. Emery et al. (1998) observed an enhanced response to light pulses for phase shifting in overexpressors of dcry. Ishikawa et al. (1999) observed a decreased response. An assay based on Aschoff’s rule (Aschoff, 1979) has also been used definitively to demonstrate the role of cryptochrome as a circadian photoreceptor. In D. melanogaster, period length in constant light increases with increasing fluence rate to the extent that, at very high intensities of light, wild-type flies become arrhythmic (Aschoff, 1979; Konopka et al., 1989). Mutant cryb flies do not respond to this increasing fluence rate and continue to display strong rhythmicity even in intense constant illumination. This indicates that circadian photoperception is completely impaired in the absence of cryptochrome (Emery et al., 2000). A wild-type phenotype can be restored in the cryb mutant flies by expression of wild-type dCRY in lateral neuron cells. dCRY is thus demonstrated to be the only circadian photoreceptor that impinges directly on the clock in D. melanogaster (Emery et al., 2000). This leaves a question as to how the visual photoreceptors can entrain the clock in a cryb mutant. It was proposed by Emery et al. (2000) that visual stimuli may act to drive a rhythm of physical activity in light/dark cycles and that this, in turn, somehow feeds back to entrain the behavioural rhythm that can subsequently be observed in cryb flies under constant conditions.
The mode of action of dCRY in resetting the clock at the molecular level was identified by Ceriani et al. (1999). Using a yeast two-hybrid assay, dCRY was shown to interact directly with TIM. This interaction was observed in the light, but not in darkness, pointing to a light-dependent interaction of dCRY with the PER-TIM dimer (Ceriani et al., 1999). Furthermore, in a D. melanogaster cell culture system, dCRY was found to negate the action of the PER-TIM dimer in feeding back on per and tim transcription in light but not in darkness, effectively resetting the clock to a point at which per and tim transcription are high (Ceriani et al., 1999).
The D. melanogaster cryptochrome dcry shows a circadian rhythm of expression with a peak in the later part of the day. As is proposed to be the case for the plant photoreceptors, this oscillation may modulate light resetting of the clock and affect the shape of the phase response curve (Ishikawa et al., 1999) (Fig. 6).
In a recent study by Krishnan et al. (2001), a further role for dCRY in the D. melanogaster clock was proposed. In addition to the role of dCRY as the circadian photoreceptor in D. melanogaster brain, Krishnan et al. (2001) showed that dCRY may be part of the oscillator mechanism itself in peripheral tissue. A circadian rhythm of olfactory responses can be observed in the antennae of D. melanogaster. In wild-type flies maintained in constant darkness, this rhythm could be entrained by temperature cycles, but such temperature cycles were unable to entrain the rhythm in cryb flies. This suggests either that dCRY is essential for temperature entrainment in D. melanogaster or that it forms part of the oscillator mechanism in the antenna. As there is no precedent of dCRY having a thermoreceptive role, the latter seems more likely. This result stresses the care that needs to be exercized when denoting a particular gene/protein as a photoreceptor or clock component.
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Photoreceptors involved in light input to the circadian clock in mammals |
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In mammals, cryptochrome plays an integral role in the central clock mechanism. Two cryptochromes, CRY1 and CRY2 exist in mammals (Devlin and Kay, 1999), though it is uncertain whether they play a role within light input to the clock. In mice, the clock mechanism is made up of a similar transcriptional feedback loop to that discovered in insects, though CRY replaces TIM within the mammalian system and there are three per genes present (Kume et al., 1999; Field et al., 2000; Reppert and Weaver, 2001). Transcription of the mCry and mPer genes begins in the late afternoon and levels of the proteins in the cytoplasm rise steadily. mCRY–mCRY dimers or mCRY–mPER dimers then form, enabling their entry into the nucleus where these dimers inhibit the action of their own transcriptional activators, CLK and CYC, and thus exert a negative feedback on their own transcription so that levels of cry and per subsequently fall again. It appears that inhibition of the CLK–CYC complex is effected largely by the CRY proteins, thus the role of CRY has become central to the clock mechanism itself (Reppert and Weaver, 2001). Consistent with this, mCry1–/– mCry2–/– mice are arrhythmic in constant light (van der Horst et al., 1999). Again a second, interlocking feedback loop exists. In this case mPER2 acts as a promoter of CYC transcription, whilst mCRY plays a role in stabilizing mPER2 (Shearman et al., 2000).
Some evidence points to a role for cry in light input to the mammalian clock, though this is not definitive. It is difficult to prove a role for CRY in light input to the mammalian clock based on studies of the mCry1–/– mCry2–/– double mutant mice as the clock itself no longer runs in these mutants (van der Horst et al., 1999). Evidence for altered response to phase-shifting pulses of light has been demonstrated for the mCry2–/– monogenic mutants. mCry2–/– mutant mice show an enhanced response to a phase-shifting light pulse during the subjective night (Thresher et al., 1998). One of the early events associated with phase resetting in response to a light pulse is a rapid induction of mPer1. mCry1–/– and mCry2–/– monogenic mutants display aberrant mPer1 induction (Vitaterna et al., 1999). Studies of light-induced mPer1 transcription in mCry1–/– mCry2–/– double mutant mice also suggest a role for mCRY as a circadian photoreceptor. mCry1–/– mCry2–/– double mutant mice fail to show mPer1 induction in response to a light pulse given during the night. However, if mCry1–/– mCry2–/– mutants are left in darkness for 52 h prior to a light pulse, then light-induction of mPer1 is observed, suggesting the action of another, possibly light-labile, photoreceptor (Okamura et al., 1999). In addition, mPer2 is still induced in response to a light pulse in mCry1–/– mCry2–/– mutants and, whilst induction of mPer2 has not been shown to lead to clock resetting, this also indicates the involvement of photoreceptors other than cryptochrome acting upon the clock system (Vitaterna et al., 1999).
mCRYs do play a role as photoreceptors for behavioural modification in mice. As well as showing a circadian regulation of locomotor activity, whereby they are active during the subjective night and inactive during the subjective day, wild-type mice show a simple responsive behaviour to light/dark cycles whereby they remain inactive whenever the light is on. The cryptochromes have been shown to act redundantly with the classical retinal photoreceptors in the perception of light in the control of this response (Selby et al., 2000). This result indicates that they can act as photoreceptors and that they do play a dual role, both as part of the clock mechanism and as photoreceptors in their own right. Whether they contribute to circadian photoperception will be more difficult to ascertain.
It is certain, however, that the mammalian circadian photoreceptor is located in the eye as enucleation results in loss of circadian entrainment (Foster, 1998). Experiments with rodless and coneless rats, however, have demonstrated that neither rods nor cones are essential for clock resetting (Freedman et al., 1999). mCRY is found in the retinal ganglion layer of the eye, thus cryptochrome is not ruled out as the ocular photoreceptor (Miyamoto and Sancar, 1998). However, it is probable that the action of a novel mammalian photoreceptor located in the eye is being witnessed. This is also suggested by the action spectrum for mammalian clock resetting which shows a peak of action at 
500 nm, corresponding better to an opsin (Provencio and Foster, 1995; Yoshimura and Ebihara, 1996) than to cryptochrome (Sancar, 2000). Novel opsins have, indeed, recently been found in Xenopus and in salmon (Soni et al., 1998; Provencio et al., 1998b).
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Differences in circadian photoperception between plants and animals |
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It is notable that the A. thaliana cry1 cry2 double mutant is still rhythmic, clearly indicating that, in A. thaliana, the cryptochromes are not essential for the running of the clock as they are in mammals but are purely involved in light input (Devlin and Kay, 2000a). The clock itself seems to have evolved independently in plants and in animals and, although much of the clock ‘mechanism’ appears conserved between insects and mammals (Willaims and Sehgal, 2001), these components have not been found in plants. It is, therefore, no surprise that the circadian photoreceptors also arose independently in plants and animals, but it remains an interesting observation that, in both cases, molecules derived from the blue-light sensing photolyases are closely involved with the clock.
Another distinct feature of plant and animal clocks is that, whilst in animals there is a strong central co-ordination of circadian oscillations throughout the organism mediated via the brain, in plants there appears to be no such co-ordination. Within mammals a region of the hypothalamus known as the suprachiasmatic nucleus (SCN) acts as a central clock regulating rhythms throughout the rest of the body (Yamazaki et al., 2000). The SCN shows a direct synaptic connection to the eyes, thought to be the route of clock resetting light signals (Provencio et al., 1998a). Whilst rhythms can be maintained in isolated mammalian tissues, clock resetting by light has not been demonstrated in these peripheral tissues and appears to require central control via signals from the SCN (Sakamoto et al., 1998; Yamazaki et al., 2000). Within flies the central control appears to be exhibited by the lateral neurones (Stanewsky et al., 1998). Rhythmic expression of the clock genes within the lateral neurones alone has been demonstrated to be sufficient to maintain locomotor rhythms of the whole fly (Stanewsky et al., 1998). Isolated body parts of D. melanogaster can also maintain rhythmic clock gene expression and, furthermore, can be entrained by light signals indicating that, although the clock is controlled centrally in flies, clock resetting throughout the organism is not absolutely dependent on signals from the lateral neurones (Plautz et al., 1997). In plants, it has been demonstrated the intact cotyledons on the same plant can be stably entrained to different light/dark cycles independently and will continue to cycle out-of-phase when transferred back to constant conditions (Thain et al., 2000). This indicates that not only is each part of the plant capable of independent clock resetting but that there is no systemic co-ordination of the clock throughout the plant as a whole. All co-ordination of rhythms throughout the plant is therefore dependent on each part of the plant detecting the same environmental signals.
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Photoreceptors involved in light input to the circadian clock in fungi |
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Yet another independently evolved clock mechanism is found in the fungus, Neurospora crassa. N. crassa formed a model organism in which many of the principles of an oscillator based on a transcriptional feedback loop were established (Dunlap, 1999). The frequency (frq) gene of N. crassa forms part of a self-sustaining oscillator whereby the FRQ protein feeds back on frq transcription (Aronson et al., 1994). In N. crassa two proteins, WHITECOLLAR 1 and 2 (WC-1 and WC-2), that are required for all known photoresponses, have been shown to be essential for light input to the clock (Harding and Melles, 1983; Russo, 1988; Sommer et al., 1989; Lauter and Russo, 1991; Arpaia et al., 1993). WC-1 and WC-2 act as positive regulators that maintain robust FRQ cycling (Crosthwaite et al., 1997). WC-1 and WC-2 form a transactivating complex known as the whitecollar complex (WCC) which activates frq transcription (Ballario et al., 1998; Talora et al., 1999; Denault et al., 2001). As FRQ protein subsequently rises, the FRQ protein interacts directly with this complex to negate its action on the frq promoter so that FRQ protein is no longer produced and the levels of FRQ subsequently fall again (Denault et al., 2001). WC-1 is responsible for the light induction of the frq transcript that results in a phase shift in the rhythm (Crosthwaite et al., 1997). Interestingly, the WC-1 is also rhythmically expressed under the control of FRQ protein (Denault et al., 2001). As with the oscillating light input components in A. thaliana and D. melanogaster this may form a mechanism of gating of the light responsiveness of the clock to appropriate times of day. Very recently a further putative gating component was identified in N. crassa. The protein, VIVID (VVD) regulates the light response in N. crassa (Heintzen et al., 2001). VVD forms an independent autoregulatory transcriptional feedback loop. Transcription of vvd is regulated by the WCC and VVD protein is rapidly induced by light. The VVD protein then acts to negate the WCC, effectively reducing the light responsiveness of N. crassa. Consequently, vvd mutants of N. crassa show severely dampened gating and an alteration in the phase response curve (Heintzen et al., 2001) (Fig. 7).
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Temperature input to the clock |
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The response of the circadian clock to temperature shows something of a paradox. The clock exhibits a temperature compensation whereby, under constant conditions, the period length of the rhythm is almost unaffected by the external temperature. The phenomenon of temperature compensation was first observed by Pittendrigh (1954) studying the eclosion rhythm of Drosophila pseudoobscura pupae. He found that this rhythm maintains the same period length over a wide range of temperature. Similarly, the rhythms studied in plants show very low sensitivity to temperature (Salisbury et al., 1968; Somers et al., 1998b). For most biochemical reactions the rate will increase 2–3-fold for a 10 °C increase in temperature (Q10=2–3). CAB::LUC rhythms in A. thaliana show a slight shortening of period length in response to increasing temperature with a Q10 of 1.0–1.1 (Somers et al., 1998b).
However, despite the temperature compensation which is built into the endogenous clock, a sudden temperature change is able to act as a Zeitgeber and entrain the clock to a new phase. Clocks can, in fact, be entrained to a temperature rhythm such as that which occurs with the day/night cycle in the natural environment (Bünning, 1973; Somers et al., 1998b; Merrow et al., 1999), though much less is known about the temperature input to the clock in entrainment.
Temperature entrainment has been used experimentally to examine the position of mutations within the clock system. The frq null mutant of N. crassa shows an arrhythmic phenotype in constant conditions. The frq null fails to entrain to light/dark cycles, but will stably entrain to temperature cycles, suggesting that frq is a critical clock component essential for light-mediated entrainment of circadian rhythms in N. crassa (Merrow et al., 1999). It appears that another frq-independent oscillator is responsible for the rhythms observed in frq mutants in response to temperature entrainment (Roenneberg and Merrow, 2000). Such a frq-independent oscillator had also previously been proposed on the basis that the frq null mutant will eventually display a (very long period) rhythm after an extended period in constant conditions (Loros and Feldman, 1986). Curiously, wc-1 and wc-2 mutants cannot be entrained by either light or temperature indicating a wider involvement in the clock (Crosthwaite et al., 1997).
Similarly temperature entrainment was used to demonstrate that the elf3 mutant of A. thaliana specifically affects light input to the oscillator. As discussed earlier, the elf3 mutant has lost gating light signalling causing the action of the oscillator to be masked in continuous light (McWatters et al., 2000). Temperature entrainment can restore rhythmicity in the elf3 mutant demonstrating that the mutation specifically affects the light input pathway to the clock (McWatters et al., 2000).
Temperature cycles were used to demonstrate that the toc1 mutation in A. thaliana lies within the central oscillator as opposed to being in an input pathway (Somers et al., 1998b). The toc1 mutant displays a short period length for a number of rhythmic outputs even in darkness indicating that it does not lie in the light input pathway (Somers et al., 1998b). toc1 was shown not to affect temperature compensation and following temperature entrainment the toc1 mutant also showed a short period length. Furthermore, in cycles of alternating high and low temperature, the peak of CAB::LUC expression in the toc1 mutant led that of the wild type (Somers et al., 1998b). A feature of mutants affecting the period length of the clock is that the timing of the peak of the rhythm relative to the entraining signal will differ from that seen in the wild type. In a short period mutant the peak will lead that of the wild type and in a long period mutant the peak will lag behind that of the wild type. Thus the toc1 mutant does not affect the process of temperature entrainment of the clock and so does not lie within the temperature input pathway. toc1 is, therefore, proposed to affect the oscillator mechanism itself (Somers et al., 1998b).
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Conclusions |
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A common feature of circadian systems in all species examined is the close association between light input and the oscillator itself. Several systems display an oscillation in expression of the circadian photoreceptors themselves. Phytochrome B in A. thaliana shows a circadian rhythm of transcription with a peak in the late part of the night/early morning (Bognar et al., 1999; Harmer et al., 2000). The A. thaliana cryptochromes oscillate with a peak in the late part of the day (Harmer et al., 2000). D. melanogaster cryptochrome also shows a circadian oscillation with a peak in the late part of the day (Ishikawa et al., 1999). Interestingly, whilst it is uncertain whether the mammalian cryptochromes are circadian photoreceptors their expression also oscillates under circadian control. mCry1 oscillates with a circadian rhythm in the SCN, also showing a peak in the late part of the day, whilst both mCry1 and mCry2 oscillate with a circadian rhythm in peripheral skeletal tissue (Kume et al., 1999).
Clearly the output from the clock feeds back to regulate input. As well as direct regulation of photoreceptor levels a gating or modulation of responsivity to signals from the photoreceptors is an integral part of many circadian systems. This can regulate the degree of clock resetting in response to the signals from the light environment at different times of day (Roenneberg and Foster, 1997). This feature of these clocks means that they will respond most strongly to environmental conditions at crucial times of day, namely dawn and/or dusk when the acquisition of information about the light environment is most important. Recently, elements involved in gating responses have begun to be characterized (McWatters et al., 2000; Heintzen et al., 2001). The elucidation of such regulatory gating or modulating mechanisms will be important for the full understanding of the central oscillator itself. It may even be hypothesized that a feedback loop modulating the activity of a photoreceptor could have been at the very origin of circadian clocks.
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References |
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Ahmad M, Cashmore AR. 1993. HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor. Nature 366, 162–166.[Medline]
Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Mas P, Kay SA. 2001. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293, 880–883.
Allada R, White NE, So WV, Hall JC, Rosbash M. 1998. A mutant Drosophila homolog of mammalian Clock disrupts circadian rhythms and transcription of period and timeless. Cell 93, 791–804.[Web of Science][Medline]
Aronson BD, Johnson KA, Loros JJ, Dunlap JC. 1994. Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263, 1578–1584.
Arpaia G, Loros JJ, Dunlap JC, Morelli G, Macino G. 1993. The interplay of light and the circadian clock. Plant Physiology 102, 1299–1305.[Abstract]
Aschoff J. 1979. Circadian rhythms: influences of internal and external factors on the period measured in constant conditions. Zeitschrift für Tierpsychologie 49, 225–249.[Web of Science][Medline]
Ballario P, Talora C, Galli D, Linden H, Macino G. 1998. Roles in dimerization and blue light photoresponse of the PAS and LOV domains of Neurospora crassa white collar proteins. Molecular Microbiology 29, 719–729.[Web of Science][Medline]
Bognar LK, Hall A, Adam E, Thain SC, Nagy F, Millar AJ. 1999. The circadian clock controls the expression pattern of the circadian input photoreceptor, phytochrome B. Proceedings of the National Academy of Sciences, USA 96, 14652–14657.
Bünning E. 1973. The physiological clock, New York: Springer.
Carré IA, Kim J-Y. 2002. MYB transcription factors in the Arabidopsis circadian clock. Journal of Experimental Botany 53, 1551–1557.
Cashmore AR, Jarillo JA, Wu YJ, Liu D. 1999. Cryptochromes: blue light receptors for plants and animals. Science 284, 760–765.
Ceriani MF, Darlington TK, Staknis D, Mas P, Petti AA, Weitz CJ, Kay SA. 1999. Light-dependent sequestration of TIMELESS by CRYPTOCHROME. Science 285, 553–556.
Christie JM, Briggs WR. 2001. Blue light sensing in higher plants. Journal of Biological Chemistry 276, 11457–11460.
Christie JM, Reymond P, Powell GK, Bernasconi P, Raibekas AA, Liscum E, Briggs WR. 1998. Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282, 1698–1701.
Clack T, Mathews S, Sharrock RA. 1994. The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Molecular Biology 25, 413–427.[Web of Science][Medline]
Crosthwaite SK, Dunlap JC, Loros JJ. 1997. Neurospora wc-1 and wc-2: Transcription, photoresponses, and the origins of circadian rhythmicity. Science 276, 763–769.
Crosthwaite SK, Loros JJ, Dunlap JC. 1995. Light-induced resetting of a circadian clock is mediated by a rapid increase in frequency transcript. Cell 81, 1001–1012.
Darlington TK, Wager-Smith K, Ceriani MF, Staknis D, Gekakis N, Steeves TDL, Weitz CJ, Takahashi JS, Kay SA. 1998. Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science 280, 1599–1603.
Darwin C. [1895] 1981. The power of movement in plants. New York: D Appleton and Co.
de Mairan J. 1729. Observation botanique. Histoire de l’Academie Royale des Sciences, 35–36.
Denault DL, Loros JJ, Dunlap JC. 2001. WC-2 mediates WC-1-FRQ interaction within the PAS protein-linked circadian feedback loop of Neurospora. EMBO Journal 20, 109–117.[Web of Science][Medline]
Devlin PF, Kay SA. 1999. Cryptochromes—bringing the blues to circadian rhythms. Trends in Cell Biology 9, 295–298.[Web of Science][Medline]
Devlin PF, Kay SA. 2000a. Cryptochromes are required for phytochrome signaling to the circadian clock but not for rhythmicity. The Plant Cell 12, 2499–2510.
Devlin PF, Kay SA. 2000b. Flower arranging in Arabidopsis. Science 288, 1600–1602.
Devlin PF, Kay SA. 2001. Circadian photoperception. Annual Review of Physiology 63, 677–694.[Web of Science][Medline]
Duffield GE, Best JD, Meurers BH, Bittner A, Loros JJ, Dunlap JC. 2002. Circadian programs of transcriptional activation, signalling and protein turnover revealed by microarray analysis of Mammalian cells. Current Biology 12, 551–557.[Web of Science][Medline]
Dunlap JC. 1999. Molecular bases for circadian clocks. Cell 96, 271–290.[Web of Science][Medline]
Edmunds LN. 1988. Cellular and molecular bases of biological clocks. New York: Springer-Verlag.
Emery P, Stanewsky R, Hall JC, Rosbash M. 2000. A unique circadian-rhythm photoreceptor. Nature 404, 456–457.[Medline]
Emery PT, So WV, Kaneko M, Hall JC, Rosbash M. 1998. CRY, a Drosophila clock and light-regulated cryptochrome, is a major contributor to circadian rhythm resetting and photosensitivity. Cell 95, 669–679.[Web of Science][Medline]
Engelmann W, Simon K, Phen CJ. 1994. Leaf movement in Arabidopsis thaliana. Zeitschrift für Naturforschung 47, 925–928.3
Enright JT. 1982. Sleep movements of leaves: in defense of Darwin’s interpretation. Oecologia 54, 253–259.[Web of Science]
Field MD, Maywood ES, O’Brien JA, Weaver DR, Reppert SM, Hastings MH. 2000. Analysis of clock proteins in mouse SCN demonstrates phylogenetic divergence of the circadian clockwork and resetting mechanisms. Neuron 25, 437–447.[Web of Science][Medline]
Foster RG. 1998. Shedding light on the biological clock. Neuron 20, 829–832.[Web of Science][Medline]
Freedman MS, Lucas RJ, Soni B, von Schantz M, Munoz M, David-Gray Z, Foster R. 1999. Regulation of mammalian circadian behaviour by non-rod, non-cone ocular photoreceptors. Science 284, 502–504.
Glossop NR, Lyons LC, Hardin PE. 1999. Interlocked feedback loops within the Drosophila circadian oscillator. Science 286, 766–768.
Hall JC. 2000. Cryptochromes: sensory reception, transduction, and clock functions subserving circadian systems. Current Opinion in Neurobiology 10, 456–466.[Web of Science][Medline]
Harding RW, Melles S. 1983. Genetic analysis of phototropism of Neurospora crassa perithecial beaks using white collar and albino mutants. Plant Physiology 72, 996–1000.
Harmer SL, Hogenesch JB, Straume M, Chang HS, Han B, Zhu T, Wang X, Kreps JA, Kay SA. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290, 2110–2113.
Heintzen C, Loros JJ, Dunlap JC. 2001. The PAS protein VIVID defines a clock-associated feedback loop that represses light input, modulates gating, and regulates clock resetting. Cell 104, 453–464.[Web of Science][Medline]
Hicks KA, Millar AJ, Carré IA, Somers DE, Straume M, Meeks-Wagner R, Kay SA. 1996. Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274, 790–792.
Hirschfeld M, Tepperman JM, Clack T, Quail PH, Sharrock RA. 1998. Coordination of phytochrome levels in phyB mutants of Arabidopsis as revealed by apoprotein-specific monoclonal antibodies. Genetics 149, 523–535.
Huala E, Oeller PW, Liscum E, Han IS, Larsen E, Briggs WR. 1998. Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278, 2120–2123.[Web of Science]
Ishikawa T, Matsumoto A, Kato Jr T, Togashi S, Ryo H, Ikenaga M, Todo T, Ueda R, Tanimura T. 1999. DCRY is a Drosophila photoreceptor protein implicated in light entrainment of circadian rhythm. Genes to Cells 4, 57–65.[Abstract]
Jarillo JA, Ahmad M, Cashmore AR. 1998. A second member of the NPH serine/threonine kinase family of Arabidopsis. Plant Physiology 117, 719.
Jarillo JA, Capel J, Tang RH, Yang HQ, Alonso JM, Ecker JR, Cashmore AR. 2001. An Arabidopsis circadian clock component interacts with both CRY1 and phyB. Nature 410, 487–490.[Medline]
Johnson CH. 1990. PRC Atlas. http://johnsonlab.biology.vanderbilt.edu/prcatlas/prcatlas.html
Johnson E, Bradley M, Harberd NP, Whitelam GC. 1994. Photoresponses of light-grown phyA mutants of Arabidopsis. Phytochrome A is required for the perception of daylength extensions. Plant Physiology 105, 141–149.[Abstract]
Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M. 2001. Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291, 2138–2141.
Kendrick RE, Kronenberg GHM. (eds.) 1994. Photomorphogenesis in plants. Dordrecht: Kluwer Academic Plublishers.
Kircher S, Kozma-Bognar L, Kim L, Adam E, Harter K, Schafer E, Nagy F. 1999. Light quality-dependent nuclear import of the plant photoreceptors phytochrome A and B. The Plant Cell 11, 1445–1456.
Kiyosue T, Wada M. 2000. LKP1 (LOV kelch protein 1): a factor involved in the regulation of flowering time in Arabidopsis. The Plant Journal 23, 807–815.[Web of Science][Medline]
Konopka RJ, Pittendrigh CS, Orr D. 1989. Reciprocal behavior associated with altered homeostasis and photosensitivity of Drosophila clock mutants. Journal of Neurogenetics 6, 1–10.[Medline]
Krishnan B, Levine JD, Lynch MK, Dowse HB, Funes P, Hall JC, Hardin PE, Dryer SE. 2001. A new role for cryptochrome in a Drosophila circadian oscillator. Nature 411, 313–317.[Medline]
Kume K, Zylka MJ, Sriram S, Shearman LP, Weaver DR, Jin X, Maywood ES, Hastings MH, Reppert SM. 1999. mCRY1 and mCRY2 are essential components of the negative limb of the circadian clock feedback loop. Cell 98, 193–205.[Web of Science][Medline]
Lauter FR, Russo VE. 1991. Blue light induction of conidiation-specific genes in Neurospora crassa. Nucleic Acids Research 19, 6883–6886.
Lin C, Robertson DE, Ahmad M, Raibekas AA, Jorns MS, Dutton PL, Cashmore AR. 1995. Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1. Science 269, 968–970.
Lin C, Yang HY, Guo HW, Mockler T, Chen J, Cashmore AR. 1998. Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proceedings of the National Academy of Sciences, USA 95, 2690.
Liscum E, Briggs WR. 1995. Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. The Plant Cell 7, 473–485.[Abstract]
Loros JJ, Feldman JF. 1986. Loss of temperature compensation of circadian period length in the frq-9 mutant of Neurospora crassa. Journal of Biological Rhythms 1, 187–198.
Luce GG. 1971. Biological rhythms in human and animal physiology. New York: Dover Publications.
Malhotra K, Kim S-T, Batschauer A, Dawut L, Sancar A. 1995. Putative blue-light photoreceptors from Arabidopsis thaliana and Sinapis alba with a high degree of sequence homology to DNA photolyase contain the two photolyase cofactors but lack DNA repair activity. Biochemistry 34, 6892–6899.[Medline]
Martinez-Garcia JF, Huq E, Quail PH. 2000. Direct targeting of light signals to a promoter element-bound transcription factor. Science 288, 859–863.
Mathews S, Sharrock RA. 1997. Phytochrome gene diversity. Plant, Cell and Environment 20, 666–671.
McDonald MJ, Rosbash M. 2001. Microarray analysis and organization of circadian gene expression in Drosophila. Cell 107, 567–578.[Web of Science][Medline]
McWatters HG, Bastow RM, Hall A, Millar AJ. 2000. The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408, 716–720.[Medline]
Merrow M, Brunner M, Roenneberg T. 1999. Assignment of circadian function for the Neurospora clock gene frequency. Nature 399, 584–586.[Medline]
Millar AJ, Carré IA, Strayer CA, Chua N-H, Kay SA. 1995a. Circadian clock mutants in Arabidopsis identified by luciferase imaging. Science 267, 1161–1163.
Millar AJ, Kay SA. 1991. Circadian control of cab gene transcription and mRNA accumulation in Arabidopsis. The Plant Cell 3, 541–550.
Millar AJ, Kay SA. 1996. Integration of circadian and phototransduction pathways in the network controlling CAB gene transcription in Arabidopsis. Proceedings of the National Academy of Sciences, USA 93, 15491–15496.
Millar AJ, Short SR, Chua N-H, Kay SA. 1992. A novel circadian phenotype based on firefly luciferase expression in transgenic plants. The Plant Cell 4, 1075–1087.
Millar AJ, Straume M, Chory J, Chua N-H, Kay SA. 1995b. The regulation of circadian period by phototransduction pathways in Arabidopsis. Science 267, 1163–1166.
Miyamoto Y, Sancar A. 1998. Vitamin B2-based blue-light photoreceptors in the retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. Proceedings of the National Academy of Sciences, USA 95, 6097–6102.
Moore-Ede CM, Sulzman FM, Fuller CA. 1982. The clocks that time us. Cambridge: Harvard University Press.
Nelson DC, Lasswell J, Rogg LE, Cohen MA, Bartel B. 2000. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell 101, 331–340.[Web of Science][Medline]
Nelson DE, Takahashi JS. 1991. Sensitivity and integration in a visual pathway for circadian entrainment in the hamster (Mesocricetus auratus). Journal of Physiology 439, 115–145.
Ni M, Tepperman JM, Quail PH. 1998. PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix–loop–helix protein. Cell 95, 657–667.[Web of Science][Medline]
Ni M, Tepperman JM, Quail PH. 1999. Binding of phytochrome B to its nuclear signalling partner PIF3 is reversibly induced by light. Nature 400, 781–784.[Medline]
Okamura H, Miyake S, Sumi Y, Yamaguchi S, Yasui A, Muijtjens M, Hoeijmakers JH, van der Horst GT. 1999. Photic induction of mPer1 and mPer2 in cry-deficient mice lacking a biological clock. Science 286, 2531–2534.
Pittendrigh CS. 1954. On temperature independence in the clock system controlling emergence time in Drosophila. Proceedings of the National Academy of Sciences, USA 40, 1018–1029.
Plautz JD, Kaneko M, Hall JC, Kay SA. 1997. Independent photoreceptive circadian clocks throughout Drosophila. Science 278, 1632–1635.
Provencio I, Cooper HM, Foster RG. 1998a. Retinal projections in mice with inherited retinal degeneration: implications for circadian photoentrainment. Journal of Comparative Neurology 395, 417–439.[Web of Science][Medline]
Provencio I, Foster RG. 1995. Circadian rhythms in mice can be regulated by photoreceptors with cone-like characteristics. Brain Research 694, 183–190.[Web of Science][Medline]
Provencio I, Jiang G, De Grip WJ, Hayes WP, Rollag MD. 1998b. Melanopsin: an opsin in melanophores, brain, and eye. Proceedings of the National Academy of Sciences, USA 95, 340–345.
Quail PH. 1991. Phytochrome: a light-activated molecular switch that regulates plant gene expression. Annual Review of Genetics 25, 389–409.[Web of Science][Medline]
Reppert SM, Weaver DR. 2001. Molecular analysis of mammalian circadian rhythms. Annual Review of Physiology 63, 647–676.[Web of Science][Medline]
Roenneberg T, Foster RG. 1997. Twilight times: light and the circadian system. Photochemistry and Photobiology 66, 549–561.[Web of Science][Medline]
Roenneberg T, Merrow M. 2000. Circadian clocks: Omnes viae Romam ducunt. Current Biology 10, R742–R745.[Web of Science][Medline]
Russo VE. 1988. Blue light induces circadian rhythms in the bd mutant of Neurospora: double mutants bd,wc-1 and bd,wc-2 are blind. Journal of Photochemistry and Photobiology 2, 59–65.
Rutila JE, Suri V, Le M, So WV, Rosbash M, Hall JC. 1998. CYCLE is a second bHLH-PAS clock protein essential for circadian rhythmicity and transcription of Drosophila period and timeless. Cell 93, 805–814.[Web of Science][Medline]
Sakamoto K, Nagase T, Fukui H, Horikawa K, Okada T, Tanaka H, Sato K, Miyake Y, Ohara O, Kako K, Ishida N. 1998. Multitissue circadian expression of rat period homolog (rPer2) mRNA is governed by the mammalian circadian clock, the suprachiasmatic nucleus in the brain. Journal of Biological Chemistry 273, 27039–27042.
Salisbury FB, Spomer GG, Sobral M, and Ward RT. 1968. Analysis of an alpine environment. Botanical Gazette 129, 16–32.
Sancar A. 2000. Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. Annual Review of Biochemistry 69, 31–67.[Web of Science][Medline]
Schaffer R, Ramsay N, Samach A, Corden S, Putterill J, Carré IA, Coupland G. 1998. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219–1229.[Web of Science][Medline]
Selby CP, Thompson C, Schmitz TM, Van Gelder RN, Sancar A. 2000. Functional redundancy of cryptochromes and classical photoreceptors for non-visual ocular photoreception in mice. Proceedings of the National Academy of Sciences, USA 97, 14697–14702.
Sharrock RA, Quail PH. 1989. Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes and Development 3, 1745–1757.
Shearman LP, Sriram S, Weaver DR, Maywood ES, Chaves I, Zheng B, Kume K, Lee CC, van der Horst GT, Hastings MH, Reppert SM. 2000. Interacting molecular loops in the mammalian circadian clock. Science 288, 1013–1019.
Somers DE, Devlin PF, Kay SA. 1998a. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 282, 1488–1490.
Somers DE, Schultz TF, Milnamow M, Kay SA. 2000. ZEITLUPE, a novel clock associated PAS protein from Arabidopsis. Cell 101, 319–329.[Web of Science][Medline]
Somers DE, Webb AAR, Pearson M, Kay S. 1998b. The short-period mutant, toc1-1, alters circadian clock regulation of multiple outputs throughout development in Arabidopsis thaliana. Development 125, 485–494.[Abstract]
Sommer T, Chambers JA, Eberle J, Lauter FR, Russo VE. 1989. Fast light-regulated genes of Neurospora crassa. Nucleic Acids Research 17, 5713–5723.
Soni BG, Philp AR, Foster RG, Knox BE. 1998. Novel retinal photoreceptors. Nature 394, 27–28.[Medline]
Stanewsky R, Kaneko M, Emery P, Beretta B, Wager-Smith K, Kay SA, Rosbash M, Hall JC. 1998. The cryb mutation identifies cryptochrome as a circadian photoreceptor in Drosophila. Cell 95, 681–692.[Web of Science][Medline]
Strayer C, Oyama T, Schultz TF, Raman R, Somers DE, Mas P, Panda S, Kreps JA, Kay SA. 2000. Cloning of the Arabidopsis clock gene TOC1, an autoregulatory response regulator homolog. Science 289, 768–771.
Sulzman FM. 1983. Primate circadian rhythms. Bioscience 33, 445–450.[Web of Science]
Talora C, Franchi L, Linden H, Ballario P, Macino G. 1999. Role of a white collar-1-white collar-2 complex in blue-light signal transduction. EMBO Journal 18, 4961–4968.[Web of Science][Medline]
Thain SC, Hall A, Millar AJ. 2000. Functional independence of circadian clocks that regulate plant gene expression. Current Biology 10, 951–956.[Web of Science][Medline]
Thresher RJ, Vitaterna MH, Miyamoto Y, Kazantsev A, Hsu DS, Petit C, Selby CP, Dawut L, Smithies O, Takahashi JS, Sancar A. 1998. Role of mouse cryptochrome blue-light photoreceptor in circadian photoresponses. Science 282, 1490–1494.
van der Horst GT, Muijtjens M, Kobayashi K, Takano R, Kanno S, Takao M, de Wit J, Verkerk A, Eker AP, van Leenen D, Buijs R, Bootsma D, Hoeijmakers JH, Yasui A. 1999. Mammalian Cry1 and Cry2 are essential for maintenance of circadian rhythms. Nature 398, 627–630.[Medline]
Vitaterna MH, Selby CP, Todo T, Niwa H, Thompson C, Fruechte EM, Hitomi K, Thresher RJ, Ishikawa T, Miyazaki J, Takahashi JS, Sancar A. 1999. Differential regulation of mammalian period genes and circadian rhythmicity by cryptochromes 1 and 2. Proceedings of the National Academy of Sciences, USA 96, 12114–12119.
Wager-Smith K, Kay SA. 2000. Cicadian rythym genetics: from flies to mice to humans. Nature Genetics 26, 23–27.[Web of Science][Medline]
Wang ZY, Tobin EM. 1998. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93, 1207–1217.[Web of Science][Medline]
Wheeler DA, Hamblen-Coyle MJ, Dushay MS, Hall JC. 1993. Behavior in light-dark cycles of Drosophila mutants that are arrhythmic, blind, or both. Journal of Biological Rhythms 8, 67–94.
Whitelam GC, Devlin PF. 1998. Light signalling in Arabidopsis. Plant Physiology and Biochemistry 36, 125–133.[Web of Science]
Whitelam GC, Johnson E, Peng J, Carol P, Anderson ML, Cowl JS, Harberd NP. 1993. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. The Plant Cell 5, 757–768.
Whitelam GC, Patel S, Devlin PF. 1998. Phytochromes and photomorphogenesis in Arabidopsis. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 353, 1445–1453.[Web of Science]
Willaims JA, Sehgal A. 2001. Molecular components of the circadian system in Drosophila. Annual Review of Physiology 63, 729–755.[Web of Science][Medline]
Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M, Block GD, Sakaki Y, Menaker M, Tei H. 2000. Resetting central and peripheral circadian oscillators in transgenic rats. Science 288, 682–685.
Yang Z, Emerson M, Su HS, Sehgal A. 1998. Response of the timless protein to light correlates with behavioral entrainment and suggests a non-visual pathway for circadian photoreception. Neuron 21, 215–223.[Web of Science][Medline]
Yanovsky MJ, Casal JJ, Whitelam GC. 1995. Phytochrome A, phytochrome B and HY4 are involved in hypocotyl growth responses to natural radiation in Arabidopsis: weak de-etiolation of the phyA mutant under dense canopies. Plant, Cell and Environment 18, 788–794.
Yoshimura T, Ebihara S. 1996. Spectral sensitivity of photoreceptors mediating phase-shifts of circadian rhythms in retinally degenerate CBA/J (rd/rd) and normal CBA/N (+/+) mice. Journal of Comparative Physiology A-Sensory Neural and Behavioral Physiology 178, 797–802.
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