The Circadian Clock and the Photoperiodic Control of Flowering

Dr. George Coupland:

Many physiological and developmental processes in plants and animals are under the control of the circadian clock. The clock maintains a rhythm of approximately 24 hours and many processes such as flowering of plants in response to day lengths, fungal sporulation occur as a result of the influence of the circadian clock. The phenomenon has been explained by Coupland and his associate in the Current Opinion in Plant Biology 6, 13-19. Although the rhythm is endogenous, the appropriate environmental signals at the right time are necessary in order for the circadian clock to function with the help of circadian timekeeping mechanism, called central oscillator. The latter mechanism allows them to keep pace with anticipated cyclic events in their environment. A good example is provided by some leguminous species in which leaflets, which normally fold along their mid-vein at sunset, close their leaflets on their exposure to dark clouds in the middle of the day (simulating nighttime). Recent studies have shown that in the model plant Arabidopsis thaliana, phytochromes (red light) and cryptochromes (blue light) are involved in channeling light input to the circadian clock.

Three parts of the circadian system: For convenience, the circadian system is often divided into three parts. One is the central oscillator which coordinates a circadian rhythm of approximately 24 hours. The process by which external stimuli change or reset the phase of a circadian clock is termed entrainment. The oscillator is adjusted to daily cycles, synchronizing with the advent of dawn and sunset as well as diurnal changes in temperature.

The second and third parts are input- and output pathways respectively. Establishment of synchronization is termed input pathways, while output pathways are those that are controlled by the oscillator that regulates various steps in biochemical and developmental pathways. Induction of flowering by day length is a good example of an output pathway. What is important in this context is that maximum activation of this pathway by day length occurs if the individual in question is exposed to light at the start of the dawn

In the February issue of Current Opinion in Plant Biology (vol. 6:13-19), Ryosuke Hayama and George Coupland at Max Planck Institute for Plant Breeding Research, Germany, have reviewed the current status of knowledge about the circadian clock with particular reference to recent advances in Arabidopsis .

In their introductory remarks, they describe a few recently reported clock genes such as LHY (late elongated hypocotyl), CCA1 (circadian clock associated1) and TOC1 (timing of cab (chlorophyll a/b binding) expression) isolated in ArabidopsisLHY, CCA1 and TOC1 are considered to be components of the central oscillator, which coordinate the circadian rhythm.

Fluctuation of mRNA transcripts of the clock genes: Experimental evidence indicates that there is a good deal of fluctuation in levels of mRNA transcripts of these genes. For instance, early in the morning just after dawn their levels are maximum. Analyses of CCA1 and LHY proteins have shown that they are closely related, each characterized by a single MYB-related DNA-binding motif. Overexpression of some of these genes have been found to disrupt many circadian rhythms, thereby providing evidence of their involvement in the process. With the help of a diagram, the authors have shown how CCA1 and LHY repress their own expression, when either of them is overexpressed, indicating that these genes form a negative-feedback cycle.

Regulation of circadian-clock function in Arabidopsis. Recent study has shown that multiple circadian rhythms are generated by the circadian oscillator. As a result CO (CONSTANS) which promotes flowering is activated in response to long days. This is an output that acts to regulate flowering time. Light signals also regulate CO post-transcriptionally and induce the expression of FT, a gene that promotes flowering. The expression of the ELF3 (early flowering) gene is also regulated by the circadian clock acting on light input into it. The dawn signal acting on the central oscillator resets the circadian clock, allowing the diurnal cycle to continue even under constant light.

Genes that encode phytochromes (PhyA, PhyB, PhyD, and PhyE) and cryptochromes (Cry1 and Cry2) are involved for red- and blue-light input to the clock, respectively and according to a recent finding, these genes seem to interact with those recently discovered from Arabidopsis in controlling light input into the clock. One such clock gene is ZEITLUPE (ZTL; also called ADAGIO1 [ADO1]), which affects the CABgene when it mutates by extending its expression. ZTL has been assigned to a family of three genes encoding FLAVIN-BINDING, KELCH-REPEAT, F BOX1(FKF1) and LOV KELCH PROTEIN2 (LKP2) proteins. Some recent study also indicates that the mode of action of ZTL and FKF1 genes in the control of circadian rhythms in Arabidopsis is different.

Exposure of Arabidopsis and a few other species to continuous light does not destabilize the circadian rhythm. The oscillator is considered to be a key actor that controls the diurnal cycle. The circadian clock protects it at particular times of the day, allowing the cycle to continue. Under continuous illumination, the light input to the clock is affected in early flowering Arabidopsis mutant elf3, stopping the circadian clock at a certain phase.

The authors discuss differences between ztl and some photoreceptor mutants in their ability to affect flowering time. For instance, while ztl, phyA and cry2 mutants are late flowering, those with phyB, phyD and phyE phenotypes are early flowering. The authors cite an instance of an extremely late flowering phenotype exhibited by gi (gigantea) mutants in which the light-input pathway is also impaired. These examples clearly show the complexity of the problem as to the mechanisms that operate in the control of clock genes.

Genetic control of flowering time by the circadian clock: a molecular mechanism for daylength measurement in Arabidopsis Two models explaining the operation of the circadian clock have been proposed. According to model 1, called the external coincidence model, the circadian clock sets the light-sensitive phase, implying that the promotion or inhibition of flowering is dependent upon whether or not the plant is exposed to light during that phase.

According to the second model, called the internal coincidence model, flowering is promoted or inhibited in response to environmental cues, dependent upon whether the two rhythms are brought to function into the same phase. Interestingly, the two rhythms, even when they are out of phase, do not affect flowering.

Describing the role of the flowering-time gene CO, the authors compare its effects on the elf3- (early flowering) and the LHY (late elongated hypocotyl) gene. While elf3 increases CO expression, the overexpression of LHY delays flowering. Furthermore, the pleiotropic effect of the early flowering trait over late-flowering phenotypes was observed, signifying that CO plays a significant role in controlling the effect of the circadian clock on the flowering time of Arabidopsis.

Activation of FLOWERING LOCUS T by Constans: The authors describe another important role of CO in which it directly activates the expression of another flowering-time gene, FLOWERING LOCUS T (FT). It is only under long days (LD) that the FT gene promotes flowering. It has been shown that the expression of CO has a diurnal rhythm. The expression is maximum at dawn, resulting in enhanced levels of mRNA transcripts in the early morning. The mRNA level diminishes in the middle of the day, rising again during the night. Under short days, levels of CO mRNAs are low in the morning, rising to a higher level during the night. Thus, if light activates CO post-transcriptionally, induction of flowering may take place only under long days. This model accounts for early flowering in mutants involving the oscillator components LHY, CCA1 and TOC1 genes. Data on these mutants suggest that (a) the mutant loci turn on the expression of CO during the light phase under short-day conditions and that (b) the photoreceptors PhyA and Cry2 participate in the post-transcriptional activation of CO. Late flowering in the above mutants under LDs, provides evidence that mutations in the photoreceptor genes may have been responsible for this change of trait and is a good example of the external coincidence model.

Conclusion: The authors conclude that it remains to be seen whether mechanisms that operate in determining the photoperiodic response in Arabidopsis under LDs also hold good in case of short day plants. The chances of unraveling the operative mechanisms of circadian clock genes, have brightened up following reports (a) that proteins encoded by the CO, FT and CK2 genes in LD Arabidopsis and those encoded by the QTL Heading-date1 (Hd1), Hd3a, and Hd6 genes in SD rice are similar and (b) that the Arabidopsis flowering-time gene GI has a rice homologue.

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