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The Plant Circadian Clock and Chromatin Modifications

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The Plant Circadian Clock and Chromatin Modifications G C A T T A C G G C A T genes Review The Plant Circadian Clock and Chromatin Modifications Ping Yang 1,2, Jianhao Wang 1,2, Fu-Yu Huang 3 , Songguang Yang 1,* and Keqiang Wu 3,* 1 Key Laboratory of South China Agricultural Plant Molecular Analysis and Genetic Improvement, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China; [email protected] (P.Y.); [email protected] (J.W.) 2 University of Chinese Academy of Sciences, Chinese Academy of Sciences, Beijing 100049, China 3 Institute of Plant Biology, National Taiwan University, Taipei 106, Taiwan; [email protected] * Correspondence: [email protected] (S.Y.); [email protected] (K.W.) Received: 3 October 2018; Accepted: 5 November 2018; Published: 20 November 2018 Abstract: The circadian clock is an endogenous timekeeping network that integrates environmental signals with internal cues to coordinate diverse physiological processes. The circadian function depends on the precise regulation of rhythmic gene expression at the core of the oscillators. In addition to the well-characterized transcriptional feedback regulation of several clock components, additional regulatory mechanisms, such as alternative splicing, regulation of protein stability, and chromatin modifications are beginning to emerge. In this review, we discuss recent findings in the regulation of the circadian clock function in Arabidopsis thaliana. The involvement of chromatin modifications in the regulation of the core circadian clock genes is also discussed. Keywords: circadian clock; oscillators; transcriptional and post-transcriptional regulation; chromatin modifications; Arabidopsis 1. Introduction Plants, like animals, exhibit rhythmic biological activity, with a periodicity of 24 h. The rhythms are known as the circadian clock, which allows plants to coordinate the temporal organization of biological processes to specific times of the day or night [1]. The core components of the circadian system are oscillators, which are responsible for generating circadian rhythms. In addition to the central oscillators, the circadian system involves the input pathways that integrate oscillators’ functions with environmental timing stimuli, such as light and temperature, and the output pathways that provide a link between the oscillators and the diverse biological processes [2]. In the model plant Arabidopsis thaliana, more than 20 clock or clock-associated components are composed of interlocking transcription-translation feedback loops, which appears to be significantly more complicated than that of other model eukaryotes, such as Drosophila [3]. Different components of the circadian system act at distinct times throughout the day and night to reciprocally regulate expression of other clock genes at both the transcriptional and post-transcriptional levels (Figure1): Genes 2018, 9, 561; doi:10.3390/genes9110561 www.mdpi.com/journal/genes Genes 2018, 9, 561 2 of 11 Genes 2018, 9, x FOR PEER REVIEW 2 of 11 Figure 1.FigureMultiple 1. Multiple layers layers of of regulationregulation refine refine circadian circadian clock activity clock activityin Arabidopsis in Arabidopsisthaliana. (a). thaliana.(a). Transcriptional feedback loops at the core of the circadian oscillator in Arabidopsis: At dawn, the expression of the pseudo-responseTranscriptional feedback regulator loops (PRR)-encoding at the core of the genes; circadian GIGANTEA oscillator in (GI); Arabidopsis timing: ofAt CABdawn, expression the 1 expression of the pseudo-response regulator (PRR)-encoding genes; GIGANTEA (GI); timing of CAB (TOC1); and the evening complex EC members LUX ARRHYTHMO (LUX), NOX, and early flowering 4 expression 1 (TOC1); and the evening complex EC members LUX ARRHYTHMO (LUX), NOX, and (ELF4) wereearly repressed flowering by4 (ELF4) circadian were clockrepressed associated by circad 1ian (CCA1) clock associated and late elongated1 (CCA1) and hypocotyl late elongated (LHY). PRR9, PRR7, PRR5,hypocotyl and TOC1(LHY). are PRR9, sequentially PRR7, PRR5, expressed and TOC1 and repressare sequentially the expression expressed of CCA1and repress and LHY,the as well as their ownexpression transcription. of CCA1 and In LHY, the evening,as well as their all of own the transcription. previously In expressed the evening, components all of the previously are repressed by TOC1.expressed Subsequently, components the are EC represse maintainsd by TOC1. the repression Subsequently, of GI,the EC PRR9 maintains and PRR7. the repression (b) Protein–protein of GI, PRR9 and PRR7. (b) Protein–protein interactions among clock components: The homo- or interactions among clock components: The homo- or heterodimerization of CCA1 and LHY represses heterodimerization of CCA1 and LHY represses evening-phased genes by binding to an evening evening-phasedelement in genes their bypromoters. binding To to repress an evening gene target elements, circadian in their clock promoters. associated 1 To (CCA1) repress and gene late targets, circadianelongated clock associated hypocotyl 1(LHY) (CCA1) require and de-etiolated late elongated 1 (DET1), hypocotyl Histone deacetylase (LHY) require 6 (HDA6), de-etiolated and lysine- 1 (DET1), Histone deacetylasespecific demethylase 6 (HDA6), 1-like and 1 and lysine-specific 2 (LDL1/2) as demethylasecorepressors. Sequentially 1-like 1 and, the 2 (LDL1/2)PRRs (PRR9, as PRR7, corepressors. Sequentially,and PRR5) the PRRs bind to (PRR9, the CCA1 PRR7, and LHY and promoter PRR5) binds and torecruit the CCA1TOPOLESS and TPL LHY and promoters HDA6, thereby and recruit inhibiting the transcription of CCA1 and LHY. The interaction between TOC1 and CCA1 hiking TOPOLESS TPL and HDA6, thereby inhibiting the transcription of CCA1 and LHY. The interaction expedition (CHE) helps TOC1 bind to the promoters of CCA1 and LHY. Additionally, night light- between TOC1inducible and and CCA1 clock-regulated hiking expedition gene 1s (CHE)(LNKs) helps interact TOC1 with bind CCA1-like to the promoters5 (RVE8) and of CCA1 act as and LHY. Additionally,coactivators night light-inducibleinducing the expression and clock-regulated of TOC1. (c) Protein gene stability 1s (LNKs) and turnover interact modulate with CCA1-like the activity 5 (RVE8) and act asof coactivatorsoscillators: in the inducing afternoon, the the expression ZEITLUPE of(ZTL)-mediated TOC1. (c) Protein proteasomal stability degradation and turnover of TOC1 is modulate the activityinterrupted of oscillators: by ZTL’s in interaction the afternoon, with PRR3 the (which ZEITLUPE hinders ZTL (ZTL)-mediated access) and PRR5 proteasomal (which promotes degradation of TOC1TOC1 is interrupted translocation by to ZTL’s the nucleus). interaction On the with othe PRR3r hand, (which the phosphorylation hinders ZTL of access) PRR5 andand TOC1 PRR5 (which enhances their binding to ZTL, which promotes their degradation later in the evening. (d) The promotes TOC1 translocation to the nucleus). On the other hand, the phosphorylation of PRR5 and alternative splicing regulates activity of CCA1: under high temperatures, the SNW/ski-interacting TOC1 enhancesprotein (SKIP) their mediates binding CCA1 to ZTL, alternative which splicing, promotes leading their to degradationan aberrant spliced later form, in the CCA1 evening.β, due (d) The alternativeto splicingthe fourth regulates intron retention. activity ofCCA1 CCA1:β encodes under a highshorter temperatures, protein lacking the the SNW/ski-interacting DNA-binding Myb protein (SKIP) mediatesdomain that CCA1 is still alternative able to homo/h splicing,eterodimerize leading with to anthe aberrantfunctional splicedCCA1α and form, LHY. CCA1 However,β, due to the fourth intronCCA1 retention.β/CCA1α and CCA1 CCA1ββencodes/LHY dimers a shorter show reduced protein DNA lacking bindin theg activity DNA-binding to downstream Myb targets. domain that Under cold conditions, the accumulation of the correctly spliced variant CCA1α leads to increased is still able to homo/heterodimerize with the functional CCA1α and LHY. However, CCA1β/CCA1α and CCA1β/LHY dimers show reduced DNA binding activity to downstream targets. Under cold conditions, the accumulation of the correctly spliced variant CCA1α leads to increased CCA1 protein levels. Fully functional CCA1/CCA1 and CCA1/LHY dimers are thus able to bind to the promoters of targets. (e) Regulation of clock central oscillator TOC1 by chromatin modifications: in the morning, accumulated-CCA1/LHY, associated with the histone modification complex containing LDL1/2 and HDA6, attaches to the promoter of TOC1, thereby reducing the H3Ac and H3K4Me levels of TOC1. Consequently, TOC1 expression is low. In the evening, CCA1 and LHY expression are low, while TOC1 is highly expressed because the LDL1/2-HDA6 complex is released from the TOC1 promoter. Genes 2018, 9, 561 3 of 11 The orange star and light arch represent day and night, respectively. Ovals represent functional groups. Black bars indicate repression, and black arrows indicate the activation of transcription. Broken lines indicate relationships not proven to be direct or detected only under specific conditions 2. Transcriptional Regulation of the Circadian Clock Genes In plants, the circadian oscillator comprises the morning and evening loops that have been proposed to form a negative feedback loop to generate circadian rhythms [4]. In the morning loop, two key single-MYB-domain-containing transcription factors, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) [5] and LATE ELONGATED HYPOCOTYL (LHY) [6], together with pseudo-response regulators 5, 7, and 9 (PRR5, PRR7, and
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