Circadian Clock and Photoperiodic Flowering in Arabidopsis: CONSTANS Is a Hub for Signal Integration
Year: 2016
Type: review
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 genes (Nagel et al., 2015; Kamioka et al., 2016). This repression is partly dependent on the function of the CONSTITUTIVE PHOTOMORPHOGENIC10 (COP10)-DE-ETIOLATED1-DAMAGED DNA BINDING1 complex, a negative regulator for photomorphogenesis (Lau et al., 2011). To repress transcription, CCA1 and LHY bind to related cis-elements called Evening Element and the CCA1 Binding Site (Harmer and Kay, 2005). Chromatin immunoprecipitation sequencing analyses brought us, to our knowledge, a new insight regarding potential variation in CCA1 binding sites. In addition to Evening Element and the CCA1 Binding Site, DNA motifs that contain G-box or CT repeats are significantly enriched in the CCA1 binding regions (Nagel et al., 2015; Kamioka et al., 2016), indicating that CCA1 may form complexes with different transcription factors that alter the DNA binding preferences of complexes that contain CCA1. Previously, genetic results implied that CCA1 and LHY directly act as transcriptional activators for the morning-phased genes PSEUDO RESPONSE REGULATOR9 (PRR9) and PRR7 (Farré et al., 2005). However, recent transient induction analysis demonstrated that CCA1 can directly repress the expression of both PRR9 and PRR7 (Kamioka et al., 2016), suggesting that the previous result can be caused by indirect effects of cca1 and lhy mutations. A simplified model of the circadian clock architecture and tissue-specific expression profiles of core clock genes in Arabidopsis. A, Intricate transcriptional repression mechanisms interlocked with core clock components comprise the Arabidopsis circadian clock. In the morning, CCA1 and LHY directly bind to the promoters and repress the transcription of the clock genes expressed from midday to evening: PRR9, PRR7, PRR5, TOC1, LUX, ELF3, and ELF4. The CCA1/LHY-dependent repression is partly mediated by the interaction with COP10-DE-ETIOLATED1 (DET1)-DAMAGED DNA BINDING1 (DDB1) complex. During the day, PRR9, PRR7, and PRR5, all accompanied with TPL general repressor machinery, directly repress the expression of CCA1 and LHY. In the evening, ELF3, ELF4, and LUX form a complex referred to as the Evening Complex, and repress PRR9 and LUX transcription. LWD1, which binds to ELF3, induces PRR9, PRR5, and TOC1 expression. During the night, TOC1 reciprocally represses the core clock genes expressed from morning to evening (CCA1, LHY, PRR9, PRR7, TOC1, ELF4, and LUX) by directly binding to their promoters. As a transcriptional activator, RVE8, which peaks during the day, directly induces the expression of PRR5, TOC1, and most likely other evening-expressed genes that possess Evening Elements at their promoters. PRR5 in turn represses RVE8 transcription. LNK1 and LNK2 act as coactivators for RVE8 to induce PRR5 and TOC1. PRR5 and TOC1 proteins are subjected to 26S proteasome-mediated degradation at night by clock-associated F-box protein ZTL. Solid lines indicate transcriptional regulation, while dotted lines indicate posttranscriptional regulation. B, Daily expression profiles of clock genes show tissue specificity in long days. Solid lines represent expression patterns in vascular tissues, and dotted lines represent those in mesophyll cells. The expression profiles are drawn based on the results presented in Endo et al. (2014). From early in the morning to the first-half part of the night, PRR9, PRR7, and PRR5 redundantly repress the transcription of CCA1 and LHY via G-box-like cis-elements (Nakamichi et al., 2010, 2012; Liu et al., 2016; Fig. 1). This depression of CCA1 and LHY levels during the day allows the induction of evening-phased genes, such as those encoding EARLY FLOWERING3 (ELF3), ELF4 proteins, and LUX ARRYTHMO (LUX), a GARP-type MYB transcription factor. LUX, ELF3, and ELF4 form a protein complex referred to as the Evening Complex that represses PRR9 and LUX expression through binding to LUX binding sites in the promoters (Dixon et al., 2011; Helfer et al., 2011; Nusinow et al., 2011; Herrero et al., 2012). Affinity purification-coupled mass spectrometry analysis revealed that Evening Complex interacts not only with other clock components [TIMING OF CAB EXPRESSION1 (TOC1), and LIGHT REGULATED WD1 (LWD1), etc.] but also with red-light signaling components (all five phytochromes, and COP1, etc.) in vivo (Huang et al., 2016). Interestingly, ELF3 loses its interaction with all light-signaling components in the phytochrome B (phyB) mutant background, suggesting that the phyB-ELF3 complex is one of the signaling hubs that connects red light signaling with the circadian clock. (Huang et al., 2016). This type of biochemical approach is powerful for deciphering the complex network architecture of the clock protein interactome, as well as for discovering new regulators overlooked by genetic screening. At night, a pseudo-response regulator, TOC1 (also known as PRR1) protein becomes abundant and contributes to the repression of CCA1 and LHY transcription through binding to G-box related et al., 2012; et al., Fig. 1). In TOC1 interacts with which binds to to repress transcription of their genes et al., 2016). repression is the of the night by TOC1 protein degradation by and its and et al., et al., Fig. 1). The family of proteins also PRR5 for degradation at night et al., et al., In addition to a activators are known to in the core of the circadian clock. and two related proteins, directly act as activators of PRR9, PRR5, and TOC1 et al., et al., 2011; Fig. 1). The mutant light suggesting that also function in the light to the clock et al., 2011). activator that has been identified is Fig. 1). In the early RVE8 directly transcription of PRR5, TOC1, and likely other evening genes and 2011; et al., 2011; et al., 2012; et al., are of and Evening Element binding sites (Hsu et al., RVE8 physically interacts with and LNK2 during the day in a circadian et al., function is dependent on et al., it act as to the of can also bind to CCA1 and LHY et al., and act as repressors for genes and with RVE8 et al., 2015). that act of signaling et al., also have in the light signaling pathway. Recent revealed that the RVE8 to the model not the in the model and genes in light or regulation to be in to all of the molecular clock, this that the is not essential for function. it can of the clock to a of environmental and that the circadian clock regulates many physiological in various it be to have a and oscillator. In the we introduce this view of tissue specificity in the molecular clock. As the circadian clock can regulate many of plant and that most clock components are expressed in different tissues, it was that each a clock. with this different of can be the plant et al., that a mechanism and it of clock gene expression light et al., et al., 2012). of cells is also in but light and of and 2016). The Arabidopsis clock in the shoot can be from other in the sense that cells are to et al., 2015). In demonstrated that the clock in the shoot can circadian in tissues, the of the signaling for et al., 2015). It is that that the in clock the shoot and can be by light of clock in each tissue et al., 2016). this tissue-specific clock such as variation in clock genes, or different to has been reported in Arabidopsis plants et al., 2002; et al., et al., 2011). Recent tissue-specific analysis revealed that the clock genes in mesophyll cells and vascular cells show expression profiles from each other (Fig. Endo et al., clock in specific tissues, it can be that the vascular clock also expression of core clock genes in mesophyll cells et al., In expression of clock genes is essential for photoperiodic flowering regulation, while the circadian clock in the a crucial in et al., 2015). results that the circadian clock in each tissue contributes to specific physiological It seems that the vascular tissue a clock that may timing information for seasonal flowering. The mechanisms in phloem companion cells in leaves and Imaizumi, 2015). As the circadian clock that in the vascular is essential for photoperiodic flowering. This is a key transcriptional activator of the photoperiodic is by the circadian clock and light signaling et al., et al., et al., Complex multiple of regulation CO only induces FT environmental In this we recent in the molecular mechanisms of photoperiodic flowering, regulation related to CO and and regulation of CO is important for information into the flowering In the morning, CO transcription is by the family of proteins that bind to binding sites in the CO et al., 2005; et al., is variation in the of repeats to of the binding sites in the CO Arabidopsis the of binding sites is the of CO is and flowering time is et al., expression profiles of are directly by the circadian clock (Nakamichi et al., 2012; et al., et al., of is induced in the morning by CCA1 and LHY et al., and by PRR9, PRR7, and PRR5 in the (Nakamichi et al., 2012). The blue-light photoreceptor repression of CO transcription in the et al., et al., light through its it a complex with The complex and likely other as as for This temporal degradation of proteins in long days is by the of the circadian clock-controlled timing of and expression with of light by et al., In the of to degradation is as is expressed in the proteins are by the complex from the CO the transcriptional activators FLOWERING and bind to cis-elements in the CO to its transcription et al., 2012). are activators of CO expression in that may be other regulators of CO transcription. to transcriptional regulation, regulation of CO protein is also by intricate mechanisms (Andrés and Coupland, 2012; Shim and Imaizumi, 2015; Song et al., 2015; Fig. CO transcript is expressed from the to the dawn, but CO protein only in the in long days. To a time for CO protein plants multiple and Photoperiodic regulation of FT expression by and FT protein A, Arabidopsis plants possess multiple components to induce FT expression in the in long days. 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As also interacts with CO and CO form a complex and CO (Song et al., plants are in the the complex CO protein et al., Liu et al., et al., 2015). from CO regulation, CO activity is also by with other proteins and et al., 2014; et al., 2016; Fig. two at the but the is expressed in the morning and protein binds to CO to its of only FT expression in the proteins, and known as and also form a complex with CO to its function et al., et al., 2016). to is expressed in the morning in long days. of FT through the transcriptional repressor on the FT with form of CO for FT in the type transcription factors, OF and repress FT expression. type proteins are regulators of as are by and Song et al., also represses FT expression by physically the function of CO on the FT et al., 2015). of FT its a binding of Therefore, likely represses FT through the TPL repressor complex. also interacts with and may with the in of CO protein in the In addition to are multiple components that the transcription of FT in and Coupland, 2012; Shim and Imaizumi, 2015; Song et al., 2015). 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It was demonstrated that signaling can be integrated into the photoperiodic partly through interaction of with CO et al., 2016; et al., 2016; Fig. proteins act as negative regulators of FT expression in vascular et al., 2012). of protein of the FT in Arabidopsis et al., 2016). This be by of proteins on complex as amount of proteins results in a amount of CO and interaction et al., 2016). 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FT protein is synthesized in companion cells of leaf phloem in long it through the vascular to the shoot apical meristem and the transition from to reproductive growth et al., and 2016; Fig. proteins, and are identified as molecular of FT et al., 2012; et al., 2016; Fig. which is in the in companion and in the companion cells and interacts with FT protein in and it is for FT from companion cells to the et al., 2012). expression is not by photoperiod et al., the MYB transcription which contributes to FT expression in long is for the expression of (Abe et al., indicating the of FT induction and FT is for this is for long of FT protein through et al., 2016). expression is induced in the in long days but not in and CO is crucial for long induction of (Fig. CO physically with in the to induce its expression et al., 2016). The of FT from companion cells to the shoot apical meristem is by at two mechanisms (Fig. Therefore, photoperiodic flowering mechanisms that in companion cells also facilitate FT to the apical meristem. It has been a since we the tissue-specific of the photoperiodic time measurement mechanism CO and FT expression is to phloem companion and Until recently, it remained whether the circadian clock and also tissue-specific As in this recent demonstrated that the expression patterns of the clock genes show tissue-specific variations in Arabidopsis, and that the clock in each specific tissue each specific as it was that the vascular clock is essential for photoperiodic flowering et al., 2014; et al., 2015). As was also recently, the plant clock in each can and the et al., 2012; et al., 2015; and 2016), can circadian in clock gene transcription. to the of the genes the phloem companion cells that FT also with each other to the timing of expression of and at expressed in mesophyll cells not in vascular regulates photoperiodic flowering et al., et al., 2016), indicating the of To and in the photoperiodic we first to which gene is expressed To from specific tissue a the and be for results from of analyses is to potential for flowering time regulation. the our understanding of the molecular mechanisms of photoperiodic flowering time regulation has advanced to the identification of new regulators that CO transcriptional activity, the of changes in the FT and the characterization of components that regulate CO protein As regulation of FT is well in other plant et al., 2014; Song et al., regulation of CO activity is the important mechanism for flowering time. in the the CO as both activator and repressor of This was by light signaling perceived by but the mechanism of the remained to the regulation of CO function in this recent demonstrated that the of with other regulators likely this interacts with the protein that the plant and which is a negative regulator of flowering in long days. This interaction the repressor of et al., 2016). This is important for understanding flowering in A mechanism to the interaction may also in The which has two function by expression of et al., 2016). other show of expression with peaks in the morning or night (Huang et al., on in Arabidopsis, and may form a complex to regulate flowering time. from the of in various plant to the as well as flowering both of which be important for the of each to the environment. are to the of mechanisms in other such as plants and As multiple repressors interact with CO to repress its activity in the morning, and of the mechanisms are likely in other In mechanisms are Arabidopsis plants possess multiple mechanisms of CO in the it plants can the activity of CO on various external and internal in the in addition to regulation and Song et al., in the morning can also the function of to flowering by et al., can signals from with flowering time regulation and through the function of In of major signaling proteins, into the regulation of CO function also our view of flowering complex. of is by the circadian clock with expression in the morning et al., 2011). In addition to regulation, expression of the genes is by floral such as and et al., 2012; et al., It be of to and when of internal or external to regulate CO function to optimize flowering time to the environment. to not in this to
Source: PLANT PHYSIOLOGY
DOI: 10.1104/pp.16.01327
Authors: Jae Sung Shim, Akane Kubota, Takato Imaizumi
Institution: University of Washington
Language: English
Subfield: Plant Science
Domain: Life Sciences
Open Access status: hybrid
Estimated APC paid: $3,851
OpenAlex ID: W2525274258