Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration

Abstract

Plants sense changes in day length (= photoperiod) as a reliable seasonal cue to regulate important developmental transitions such as flowering. Integration of various external light information into the circadian clock-controlled mechanisms enables plants to precisely measure photoperiod changes in the surrounding environment. The core mechanism of photoperiodic measurement is regulation of CONSTANS (CO) activity, which takes place in phloem companion cells in leaves. Until recently, it remained unclear whether plants possess specific variations of the clock for this regulation. Now it is known that a specific circadian timing mechanism in the vascular tissue is essential for photoperiodic flowering. In addition to spatial tissue-specific regulation, temporal regulation of CO activity is also important. The identification and characterization of multiple regulators that physically interact with CO and influence its function in the morning in long days are two recent advances in photoperiodic regulation of flowering time. It seems that CO acts as a network hub to integrate various external and internal signals into the photoperiodic flowering pathway. CO regulates the amount of FLOWERING LOCUS T (FT) transcripts and FT protein moves from companion cells of leaf phloem to the shoot apical meristem. The protein that helps long-distance transport of FT protein was also identified recently. Here, we introduce recent advances in tissue-specific variations of the circadian clock and the emerging picture of the intricate connections of transcriptional regulators through CO in the morning, which all facilitate plants knowing when to flower. Properly timing the floral transition is crucial for reproductive success. It can also influence the early development of offspring. To optimize this timing, plants constantly monitor changes in the surrounding environment. Among various environmental factors, observing changes in day length (= photoperiod) is the most reliable way for many organisms to know the specific time of year. Therefore, photoperiodic regulation is one of the major flowering time mechanisms and it has been studied since it was first reported in 1920 (Song et al., 2015). Arabidopsis (Arabidopsis thaliana), as it flowers mainly in spring, can sense lengthening days to induce flowering and became a suitable model to study photoperiodic flowering regulation. (Andrés and Coupland, 2012; Song et al., 2013; Pajoro et al., 2014; Shim and Imaizumi, 2015). In principle, photoperiodic flowering mechanisms can be divided into three parts: light input, circadian clock, and output. Light information is integrated into innate photoperiodic timing mechanisms governed by the circadian clock to induce genes that trigger flowering. In flowering in Arabidopsis, light is perceived by various photoreceptors, such as the red/far-red light photoreceptor phytochrome (phy), and two classes of blue-light photoreceptors, cryptochrome (cry) and the ZEITLUPE (ZTL)/FLAVIN BINDING, KELCH REPEAT, F-BOX1 (FKF1)/LOV KELCH PROTEIN2 (LKP2) family of proteins. Photoperiodic information is ultimately converted into transcript levels of the FT gene (Song et al., 2015). FT is the florigen, as it is synthesized in leaves in long days and transported to the shoot apical meristem to start orchestrating expression of multiple floral identify genes, such as APETALA1 and LEAFY (Abe et al., 2005; Golembeski and Imaizumi, 2015). FT is mainly induced by the transcriptional activator CO in long days (Song et al., 2015). Therefore, the clock-controlled mechanism by which photoperiodic information regulates CO function is the key mechanism in Arabidopsis. In this review, we first discuss our current view of circadian clock architecture and recent advances in tissue specificity in the plant clock. Next, we introduce recent updates on photoperiodic regulation of flowering, focusing on the complex regulation of CO function. Recent genomic, biochemical, and computational approaches have greatly advanced our understanding of molecular architecture of the circadian clock in Arabidopsis (Hsu and Harmer, 2014; Shim and Imaizumi, 2015; Millar, 2016). Most clock components possess transcriptional activity, and are interconnected by time-resolved multiple feedback regulation to form this oscillator. Throughout the day, each clock gene also coordinates the expression of numerous output genes to regulate the timing of various physiological responses, such as growth and underlying metabolic regulation, hormone and stress responses, and so on (Farré and Weise, 2012; Shim and Imaizumi, 2015; Atamian and Harmer, 2016). Therefore, defects in the circadian clock have adverse effects on plant fitness (Green et al., 2002; Dodd et al., 2005). In the current model of the Arabidopsis circadian clock, most components function as repressors (Fig. 1). At dawn, two MYB transcription factors, CIRCADIAN CLOCK ASSOCIATED1 (CCA1) and LATE ELONGATED HYPOCOTYL (LHY), repress evening-phased