Evening Expression of <i>Arabidopsis GIGANTEA</i> Is Controlled by Combinatorial Interactions among Evolutionarily Conserved Regulatory Motifs

Berns, Markus Christian; Nordström, Karl; Cremer, Frédéric; Tóth, Réka; Hartke, Martin; Simon, Samson; Klasen, Jonas R.; Bürstel, Ingmar; Coupland, George

doi:10.1105/tpc.114.129437

Cited by 17 publications

(17 citation statements)

References 98 publications

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“…These data indicate that binding of the transfactor CCA1 to EE cis-elements is crucial for forming or maintaining a rhythmic pattern. EEs located upstream of TOC1 and GI are crucial for maintaining a rhythmic pattern with peaks in the evening (Harmer et al, 2000;Berns et al, 2014). Our ChIP-seq analyses indicated that there are high-resolution CCA1 binding profiles at TOC1 and GI, as well as at ELF4, LUX, and BOX, all of which are implicated in circadian clock functions (Supplemental Figure 6).…”

Section: Binding Preference Of Cca1 On a Genomic Scale In Vivomentioning

confidence: 92%

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Direct Repression of Evening Genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis Circadian Clock

et al. 2016

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The circadian clock is a biological timekeeping system that provides organisms with the ability to adapt to day-night cycles. Timing of the expression of four members of the Arabidopsis thaliana PSEUDO-RESPONSE REGULATOR (PRR) family is crucial for proper clock function, and transcriptional control of PRRs remains incompletely defined. Here, we demonstrate that direct regulation of PRR5 by CIRCADIAN CLOCK-ASSOCIATED1 (CCA1) determines the repression state of PRR5 in the morning. Chromatin immunoprecipitation followed by deep sequencing (ChIP-seq) analyses indicated that CCA1 associates with three separate regions upstream of PRR5. CCA1 and its homolog LATE ELONGATED HYPOCOTYL (LHY) suppressed PRR5 promoter activity in a transient assay. The regions bound by CCA1 in the PRR5 promoter gave rhythmic patterns with troughs in the morning, when CCA1 and LHY are at high levels. Furthermore, ChIP-seq revealed that CCA1 associates with at least 449 loci with 863 adjacent genes. Importantly, this gene set contains genes that are repressed but upregulated in cca1 lhy double mutants in the morning. This study shows that direct binding by CCA1 in the morning provides strong repression of PRR5, and repression by CCA1 also temporally regulates an evening-expressed gene set that includes PRR5.

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Section: Binding Preference Of Cca1 On a Genomic Scale In Vivomentioning

confidence: 92%

“…Gene expression data for (A) and (B) are LL12_LDHH and LDHH_ST, respectively. et al, 2000; Berns et al, 2014), were also bound by CCA1 in vivo (Supplemental Figure 6). There are also CCA1 binding site preferences around these clock-associated genes (Supplemental Figure 6).…”

Section: Binding Preference Of Cca1 On a Genomic Scale In Vivomentioning

confidence: 99%

Direct Repression of Evening Genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis Circadian Clock

et al. 2016

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“…This finding, together with the increased expression of GI in hos15-2 mutants ( Figure 1G), prompted us to investigate whether HOS15 represses GI transcription by recruiting HDACs to the GI promoter. Because GI transcription is regulated by the EC through its binding to a LUX binding site (LBS, GATWCG, where W is A or T) in the GI promoter (Berns et al, 2014;Mizuno et al, 2014), we designed two amplicons containing putative LBSs (R1 and R3) and another amplicon without a putative LBS (R2; Figure 3A). Mizuno et al (2014) showed that ELF3 and LUX associate with the GI-c region of GI, i.e., R3.…”

Section: Hos15 Is Involved In Gi-mediated Photoperiodic Floweringmentioning

confidence: 99%

HOS15 Interacts with the Histone Deacetylase HDA9 and the Evening Complex to Epigenetically Regulate the Floral Activator GIGANTEA

et al. 2019

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In plants, seasonal inputs such as photoperiod and temperature modulate the plant's internal genetic program to regulate the timing of the developmental transition from vegetative to reproductive growth. This regulation of the floral transition involves chromatin remodeling, including covalent modification of histones. Here, we report that HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE 15 (HOS15), a WD40 repeat protein, associates with a histone deacetylase complex to repress transcription of the GIGANTEA (GI)-mediated photoperiodic flowering pathway in Arabidopsis (Arabidopsis thaliana). Loss of function of HOS15 confers early flowering under long-day conditions because elevated GI expression. LUX ARRHYTHMO (LUX), a DNA binding transcription factor and component of the Evening Complex (EC), is important for the binding of HOS15 to the GI promoter. In wild type, HOS15 associates with the EC components LUX, EARLY FLOWERING 3 (ELF3), and ELF4 and the histone deacetylase HDA9 at the GI promoter, resulting in histone deacetylation and reduced GI expression. In the hos15-2 mutant, the levels of histone acetylation are elevated at the GI promoter, resulting in increased GI expression. Our data suggest that the HOS15-EC-HDA9 histone-modifying complex regulates photoperiodic flowering via the transcriptional repression of GI.

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“…GI interacts with ZTL which, in turn, regulates the stability of at least TOC1 and PRR5 (M as et al, 2003;Kim et al, 2007). The activity of GI is under clock control, including repression by EC and CCA1/ LHY and probably also activation by RVE8 (Berns et al, 2014). GI is also important for flowering time regulation through its interaction with the ZTL paralogue FLAVIN-BINDING, KELCH REPEAT, F-BOX1 (FKF1; Sawa et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Early evolution of the land plant circadian clock

et al. 2017

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Summary While angiosperm clocks can be described as an intricate network of interlocked transcriptional feedback loops, clocks of green algae have been modelled as a loop of only two genes. To investigate the transition from a simple clock in algae to a complex one in angiosperms, we performed an inventory of circadian clock genes in bryophytes and charophytes. Additionally, we performed functional characterization of putative core clock genes in the liverwort Marchantia polymorpha and the hornwort Anthoceros agrestis.Phylogenetic construction was combined with studies of spatiotemporal expression patterns and analysis of M. polymorpha clock gene mutants.Homologues to core clock genes identified in Arabidopsis were found not only in bryophytes but also in charophytes, albeit in fewer copies. Circadian rhythms were detected for most identified genes in M. polymorpha and A. agrestis, and mutant analysis supports a role for putative clock genes in M. polymorpha.Our data are in line with a recent hypothesis that adaptation to terrestrial life occurred earlier than previously expected in the evolutionary history of charophyte algae. Both gene duplication and acquisition of new genes was important in the evolution of the plant circadian clock, but gene loss has also contributed to shaping the clock of bryophytes.

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Evening Expression of Arabidopsis GIGANTEA Is Controlled by Combinatorial Interactions among Evolutionarily Conserved Regulatory Motifs

Cited by 17 publications

References 98 publications

Direct Repression of Evening Genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis Circadian Clock

Direct Repression of Evening Genes by CIRCADIAN CLOCK-ASSOCIATED1 in the Arabidopsis Circadian Clock

HOS15 Interacts with the Histone Deacetylase HDA9 and the Evening Complex to Epigenetically Regulate the Floral Activator GIGANTEA

Early evolution of the land plant circadian clock

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