Takato Imaizumi

FKF1 is essential for photoperiodic-specific light signalling in Arabidopsis.

Adaptation to seasonal change is a crucial component of an organisms survival strategy. To monitor seasonal variation, organisms have developed the capacity to measure day length (photoperiodism). Day-length assessment involves the photoperiodic control of flowering in Arabidopsis thaliana, whereby the coincidence of light and high expression of CONSTANS (CO) induces the expression of FLOWERING LOCUS T (FT), leading to flowering in long-day conditions. Although controlling CO expression is clearly a key step in day-length discrimination, the mechanism that generates day-length-dependent CO expression remains unknown. Here we show that the clock-controlled FLAVIN-BINDING, KELCH REPEAT, F-BOX (FKF1) protein has an essential role in generating the diurnal CO peak and that this function is dependent on light. We show that a recombinant FKF1 LIGHT, OXYGEN OR VOLTAGE (LOV) domain binds the chromophore flavin mononucleotide and undergoes light-induced photochemistry, indicating that FKF1 may function as a photoperiodic blue-light receptor. It is likely that the circadian control of FKF1 expression and the light regulation of FKF1 function coincide to control the daytime CO waveform precisely, which in turn is crucial for day-length discrimination by Arabidopsis.

The ELF4-ELF3-LUX complex links the circadian clock to diurnal control of hypocotyl growth

The circadian clock is required for adaptive responses to daily and seasonal changes in environmental conditions. Light and the circadian clock interact to consolidate the phase of hypocotyl cell elongation to peak at dawn under diurnal cycles in Arabidopsis thaliana. Here we identify a protein complex (called the evening complex)—composed of the proteins encoded by EARLY FLOWERING 3 (ELF3), ELF4 and the transcription-factor-encoding gene LUX ARRHYTHMO (LUX; also known as PHYTOCLOCK 1)—that directly regulates plant growth. ELF3 is both necessary and sufficient to form a complex between ELF4 and LUX, and the complex is diurnally regulated, peaking at dusk. ELF3, ELF4 and LUX are required for the proper expression of the growth-promoting transcription factors encoded by PHYTOCHROME INTERACTING FACTOR 4 (PIF4) and PIF5 (also known as PHYTOCHROME INTERACTING FACTOR 3-LIKE 6) under diurnal conditions. LUX targets the complex to the promoters of PIF4 and PIF5 in vivo. Mutations in PIF4 and/or PIF5 are epistatic to the loss of the ELF4–ELF3–LUX complex, suggesting that regulation of PIF4 and PIF5 is a crucial function of the complex. Therefore, the evening complex underlies the molecular basis for circadian gating of hypocotyl growth in the early evening.

FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering

Spring Into Flower In spring, plants respond to increasing day length and shifts in the spectrum of solar irradiance by releasing the flowering induction pathway, which includes expression of the FLOWERING LOCUS T (FT) protein. Song et al. (p. 1045) have now identified a trio of controls brought to bear on FT gene expression by the FKF1 (FLAVIN-BINDING, KELCH REPEAT, F-BOX 1) protein. FKF1 removes a repressor and also stabilizes the activating CONSTANS (CO) protein in the afternoons through a binding interaction enhanced by blue light—an increasing component of solar irradiation during spring. Then FKF1 itself helps to activate transcription of the CO gene. Thus, by removing the repressor and shoring up the activator, FKF1 sets flowering on its way. A plant protein sensitive to blue light links longer afternoons to more flowering. Plants use day-length information to coordinate flowering time with the appropriate season to maximize reproduction. In Arabidopsis, the long day–specific expression of CONSTANS (CO) protein is crucial for flowering induction. Although light signaling regulates CO protein stability, the mechanism by which CO is stabilized in the long-day afternoon has remained elusive. Here, we demonstrate that FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 (FKF1) protein stabilizes CO protein in the afternoon in long days. FKF1 interacts with CO through its LOV domain, and blue light enhances this interaction. In addition, FKF1 simultaneously removes CYCLING DOF FACTOR 1 (CDF1), which represses CO and FLOWERING LOCUS T (FT) transcription. Together with CO transcriptional regulation, FKF1 protein controls robust FT mRNA induction through multiple feedforward mechanisms that accurately control flowering timing.

Flowering time regulation: photoperiod- and temperature-sensing in leaves

Plants monitor changes in photoperiod and temperature to synchronize their flowering with seasonal changes to maximize fitness. In the Arabidopsis photoperiodic flowering pathway, the circadian clock-regulated components, such as FLAVIN-BINDING, KELCH REPEAT, F-BOX 1 and CONSTANS, both of which have light-controlled functions, are crucial to induce the day-length specific expression of the FLOWERING LOCUS T (FT) gene in leaves. Recent advances indicate that FT transcriptional regulation is central for integrating the information derived from other important internal and external factors, such as developmental age, amount of gibberellic acid, and the ambient temperature. In this review, we describe how these factors interactively regulate the expression of FT, the main component of florigen, in leaves.

Arabidopsis circadian clock and photoperiodism: time to think about location.

Plants possess a circadian clock that enables them to coordinate internal biological events with external daily changes. Recent studies in Arabidopsis revealed that tissue-specific clock components exist and that the clock network architecture also varies within different organs. These findings indicate that the makeup of circadian clock(s) within a plant is quite variable. Plants utilize the circadian clock to measure day-length changes for regulating seasonal responses, such as flowering. To ensure that flowering occurs under optimum conditions, the clock regulates diurnal CONSTANS (CO) expression. Subsequently, CO protein induces FLOWERING LOCUS T (FT) expression which leads to flowering. It is emerging that both CO and FT expression are intricately controlled by groups of transcription factors with overlapping functions.

Responses of ferns to red light are mediated by an unconventional photoreceptor

Efficient photosynthesis is essential for plant survival. To optimize photosynthesis, plants have developed several photoresponses. Stems bend towards a light source (phototropism), chloroplasts move to a place of appropriate light intensity (chloroplast photorelocation) and stomata open to absorb carbon dioxide. These responses are mediated by the blue-light receptors phototropin 1 (phot1) and phototropin 2 (phot2) in Arabidopsis (refs 1–5). In some ferns, phototropism and chloroplast photorelocation are controlled by red light as well as blue light. However, until now, the photoreceptor mediating these red-light responses has not been identified. The fern Adiantum capillus-veneris has an unconventional photoreceptor, phytochrome 3 (phy3), which is a chimaera of the red/far-red light receptor phytochrome and phototropin. We identify here a function of phy3 for red-light-induced phototropism and for red-light-induced chloroplast photorelocation, by using mutational analysis and complementation. Because phy3 greatly enhances the sensitivity to white light in orienting leaves and chloroplasts, and PHY3 homologues exist among various fern species, this chimaeric photoreceptor may have had a central role in the divergence and proliferation of fern species under low-light canopy conditions.

F-box proteins FKF1 and LKP2 act in concert with ZEITLUPE to control Arabidopsis clock progression.

In Arabidopsis thaliana, the F-box protein ZTL affects the period length of the circadian clock by regulating the stability of the core clock proteins TOC1 and PRR5. This study shows that, together with ZTL, the ZTL homologs FKF1 and LKP2 are also involved in the same protein stability regulation to determine the pace and robustness of the plant circadian clock. Regulation of protein turnover mediated by ZEITLUPE (ZTL) constitutes an important mechanism of the circadian clock in Arabidopsis thaliana. Here, we report that FLAVIN BINDING, KELCH REPEAT, F-BOX1 (FKF1) and LOV KELCH PROTEIN2 (LKP2) play similar roles to ZTL in the circadian clock when ZTL is absent. In contrast with subtle circadian clock defects in fkf1, the clock in ztl fkf1 has a considerably longer period than in ztl. In ztl fkf1 lkp2, several clock parameters were even more severely affected than in ztl fkf1. Although LATE ELONGATED HYPOCOTYL (LHY) and CIRCADIAN CLOCK ASSOCIATED1 (CCA1) expression levels are lower in ztl than in the wild type, introducing both fkf1 and lkp2 mutations into the ztl mutant dramatically diminished LHY expression without further affecting CCA1 expression. This demonstrates different contributions of ZTL, FKF1, and LKP2 in the regulation of LHY and CCA1 expression. In addition, FKF1 and LKP2 also interacted with TIMING OF CAB EXPRESSION1 (TOC1) and PSEUDO-RESPONSE REGULATOR5 (PRR5), and both proteins were further stabilized in ztl fkf1 and ztl fkf1 lkp2 compared with in ztl. Our results indicate that ZTL, FKF1, and LKP2 together regulate TOC1 and PRR5 degradation and are major contributors to determining the period of circadian oscillation and enhancing robustness.

PRR3 Is a Vascular Regulator of TOC1 Stability in the Arabidopsis Circadian Clock

The pseudoresponse regulators (PRRs) participate in the progression of the circadian clock in Arabidopsis thaliana. The founding member of the family, TIMING OF CAB EXPRESSION1 (TOC1), is an essential component of the transcriptional network that constitutes the core mechanism of the circadian oscillator. Recent data suggest a role in circadian regulation for all five members of the PRR family; however, the molecular function of TOC1 or any other PRRs remains unknown. In this work, we present evidence for the involvement of PRR3 in the regulation of TOC1 protein stability. PRR3 was temporally coexpressed with TOC1 under different photoperiods, yet its tissue expression was only partially overlapping with that of TOC1, as PRR3 appeared restricted to the vasculature. Decreased expression of PRR3 resulted in reduced levels of TOC1 protein, while overexpression of PRR3 caused an increase in the levels of TOC1, all without affecting the amount of TOC1 transcript. PRR3 was able to bind to TOC1 in yeast and in plants and to perturb TOC1 interaction with ZEITLUPE (ZTL), which targets TOC1 for proteasome-dependent degradation. Together, our results indicate that PRR3 might function to modulate TOC1 stability by hindering ZTL-dependent TOC1 degradation, suggesting the existence of local regulators of clock activity and adding to the growing importance of posttranslational regulation in the design of circadian timing mechanisms in plants.

Photoperiodic Flowering: Time Measurement Mechanisms in Leaves

Many plants use information about changing day length (photoperiod) to align their flowering time with seasonal changes to increase reproductive success. A mechanism for photoperiodic time measurement is present in leaves, and the day-length-specific induction of the FLOWERING LOCUS T (FT) gene, which encodes florigen, is a major final output of the pathway. Here, we summarize the current understanding of the molecular mechanisms by which photoperiodic information is perceived in order to trigger FT expression in Arabidopsis as well as in the primary cereals wheat, barley, and rice. In these plants, the differences in photoperiod are measured by interactions between circadian-clock-regulated components, such as CONSTANS (CO), and light signaling. The interactions happen under certain day-length conditions, as previously predicted by the external coincidence model. In these plants, the coincidence mechanisms are governed by multilayered regulation with numerous conserved as well as unique regulatory components, highlighting the breadth of photoperiodic regulation across plant species.

Similarities in the circadian clock and photoperiodism in plants

Plants utilize circadian clocks to synchronize their physiological and developmental events with daily and yearly changes in the environment. Recent advances in Arabidopsis research have provided a better understanding of the molecular mechanisms of the circadian clock and photoperiodism. One of the most important questions is whether the mechanisms discovered in Arabidopsis are conserved in other plant species. Through the identification of many Arabidopsis clock gene homologs and the characterization of some gene functions, a strong resemblance between the circadian clocks in plants has been observed. On the contrary, based on our recent increased knowledge of photoperiodic flowering mechanisms in cereals and other plants, the day-length sensing mechanisms appear to have diverged more between long-day plants and short-day plants.