Journal of Biological Rhythms
Regulation of Pol II pausing is involved in daily gene transcription in the mouse liver
Journal: Manuscript ID Manuscript Type: Date Submitted by the Author:
Journal of Biological Rhythms JBR-18-0010.R1 Original Article n/a
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Complete List of Authors:
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Manuscript Keywords:
Li, Chengwei; Wuhan University, College of Life Sciences Zhu, Jialou; Wuhan University, College of Life Sciences Gong, Changxia; Wuhan University, College of Life Sciences Li, Xiaodong; Wuhan University, College of Life Sciences circadian rhythms, biological clocks, transcription, ChIP-seq, pausing, mouse, liver
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Abstract:
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The circadian clock orchestrates gene expression rhythms. Regulation at the level of gene transcription is essential for molecular and cellular rhythms. Pol II pause release is a critical step of transcription regulation. However, whether and how Pol II pause release is regulated during daily transcription have not been characterized. In this study, we performed Pol II ChIP-seq across the day in the mouse liver, and quantitatively analyzed binding signals within the transcription start site (TSS) region and the gene body. We frequently found discordant changes between Pol II near the TSS ([Pol II]TSS, paused Pol II) and that within the gene body ([Pol II]GB, transcribing Pol II) across the genome, with only [Pol II]GB always reflecting transcription of clock and clock-controlled genes. Accordingly, Pol II traveling ratios of more than 7000 genes showed significant daily changes (> 1.5 fold). Therefore, there is widespread regulation of Pol II pausing in the mouse liver. Interestingly, gene transcription rhythms exhibited a bimodal phase distribution. The transcription of ~400 genes peaked near ZT0, coincident with a genomewide increase in [Pol II]TSS and TR. The transcription of ~300 other genes peaked ~12 hrs later, when there was a global decrease in [Pol II]TSS and TR. ChIP-seq against Tbp, a pre-initiation complex (PIC) component, revealed that Pol II recruitment mainly played an indirect role in transcriptional output, with transcriptional termination and pause release functioning prominently in determining the fate of initiated Pol II and its pausing status. Taken together, our results revealed a critical, albeit complex role of Pol II pausing control in regulating the temporal output of gene transcription.
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Title: Regulation of Pol II pausing is involved in daily gene transcription in the mouse
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liver
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Authors: Chengwei Li1, 2#, Jialou Zhu1, #, Changxia Gong1, and Xiaodong Li1,*
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Affiliations:
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College of Life Sciences, Wuhan University, Wuhan 430072, P. R. China
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Current address: Center for disease control and prevention of Linyi, Linyi, Shandong
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Province, P. R. China.
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Those authors contribute equally to this work
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Correspondence to:
[email protected]
Short Title: Daily regulation of Pol II pausing in the mouse liver
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Abstract
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The circadian clock orchestrates gene expression rhythms. Regulation at the level of gene
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transcription is essential for molecular and cellular rhythms. Pol II pause release is a critical
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step of transcription regulation. However, whether and how Pol II pause release is regulated
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during daily transcription have not been characterized. In this study, we performed Pol II
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ChIP-seq across the day in the mouse liver, and quantitatively analyzed binding signals
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within the transcription start site (TSS) region and the gene body. We frequently found
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discordant changes between Pol II near the TSS ([Pol II]TSS, paused Pol II) and that within the
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gene body ([Pol II]GB, transcribing Pol II) across the genome, with only [Pol II]GB always
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reflecting transcription of clock and clock-controlled genes. Accordingly, Pol II traveling
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ratios of more than 7000 genes showed significant daily changes (> 1.5 fold). Therefore,
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there is widespread regulation of Pol II pausing in the mouse liver. Interestingly, gene
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transcription rhythms exhibited a bimodal phase distribution. The transcription of ~400 genes
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peaked near ZT0, coincident with a genomewide increase in [Pol II]TSS and TR. The
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transcription of ~300 other genes peaked ~12 hrs later, when there was a global decrease in
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[Pol II]TSS and TR. ChIP-seq against Tbp, a pre-initiation complex (PIC) component, revealed
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that Pol II recruitment mainly played an indirect role in transcriptional output, with
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transcriptional termination and pause release functioning prominently in determining the fate
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of initiated Pol II and its pausing status. Taken together, our results revealed a critical, albeit
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complex role of Pol II pausing control in regulating the temporal output of gene transcription.
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Keywords: circadian rhythms; biological clocks; transcription; ChIP-seq; pausing; mouse;
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liver
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Introduction
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The circadian clock plays an essential role in orchestrating daily rhythms in physiology and
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behavior. With the identification of clock genes, some of which are transcription factors, the
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molecular basis of circadian timing is being revealed (Koike et al., 2012). Rhythmic
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transcription is critical for clock oscillation and for the control of cellular processes via
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rhythmic gene expression (Koike et al., 2012; Le Martelot et al., 2012; Menet et al., 2012;
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Montenegro-Montero and Larrondo, 2016). Transcription is regulated at distinct steps,
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including Pol II recruitment, initiation, pause release, transcription elongation and
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termination (Fuda et al., 2009). Despite current knowledge about the molecular clock, the
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relative roles of these steps in the daily regulation of transcription are not well characterized.
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Pol II pause release is thought as a key control step of transcription (Adelman and Lis, 2012;
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Jonkers and Lis, 2015). After the pre-initiation complex (PIC) assembles at the promoter, the
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basal transcription factor TFII H unwinds dsDNA to facilitate transcription initiation (Kim et
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al., 2000). The C-terminal domain (CTD) of Pol II is phosphorylated at Ser5 by the Cdk7
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subunit of TFII H to facilitate the recruitment of the mRNA capping enzyme (Phatnani and
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Greenleaf, 2006). Cdk7 also phosphorylates and displaces TFII E (and possibly other
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proteins), allowing the binding of DSIF (Spt4&5) and NELF (NELF-A to E) complexes to
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initiated Pol II (Larochelle et al., 2012; Nilson et al., 2015). While DSIF tethers Pol II at
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TSS-proximal regions, NELF binds to both Pol II and the nascent RNA (Yamaguchi et al.,
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2013). These two complexes, together with other factors, enable a transcriptional state termed
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pausing, where engaged Pol II is prevented from productive elongation (Adelman and Lis,
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2012;
Jonkers and Lis, 2015). While paused Pol II can be removed via transcription
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termination (at the 5’-end of genes) or released into elongation, it is relatively stable, leading
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to apparent Pol II accumulation near the TSS (Core et al., 2012; Jonkers et al., 2014).
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Disruption of DSIF or NELF does not abolish pausing, but affects transcriptional output
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(Rahl et al., 2010). The +1 nucleosome, a barrier to Pol II, is another player in Pol II pausing.
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The chromatin remodeler Chd1 is required for efficient +1 nucleosome turnover when paused
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Pol II is released into elongation (Skene et al., 2014).
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The release of paused Pol II into productive elongation requires P-TEFb (Cdk9/Cyclin T),
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which is usually sequestered in the 7SK snRNP (small nuclear ribonucleoprotein) complex
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and tethered at the TSS-proximal region (Yang et al., 2001;
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2013;
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active and can be associated with other proteins (e.g., c-Myc) (Rahl et al., 2010). The active
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P-TEFb phosphorylates NELF-E via Cdk9, causing the release of NELF from Pol II. It also
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phosphorylates Spt5, converting DSIF into an activator of Pol II elongation (Peterlin and
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Price, 2006). Cdk9 promotes the recruitment of PAF1 complex and Cdk12, the Ser2 kinase of
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elongating Pol II (Bartkowiak et al., 2010; Yu et al., 2015). Given the association of Chd1
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with elongation factors (i.e., FACT, PAF1C, and Spt5) (Skene et al., 2014), pause release can
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dissociate the NELF complex and promote the turnover of the +1 nucleosome at the same
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time. Inhibiting P-TEFb/Cdk9 mainly blocks pause release, while inhibiting Cdk12 (and
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Cdk13) preferentially affects Pol II elongation in certain genes (Jonkers et al., 2014; Zhang
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et al., 2016).
Ghamari et al., 2013; Ji et al.,
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McNamara et al., 2016). When released from the 7SK snRNP, P-TEFb becomes
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Previous studies hinted at a role for Pol II pausing in clock transcriptional oscillations. In
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Aplysia, acute application of the Cdk9 inhibitor DRB phase-shifts the clock, while its chronic
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treatment lengthens period (Raju et al., 1991). In mice, Cdk9 is associated with clock proteins
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(Padmanabhan et al., 2012). Pol II elongation is accompanied with H2A.Z incorporation into
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the +1 nucleosome (Weber et al., 2014), an event undergoing daily changes in the mouse liver
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(Menet et al., 2014). An RNAi screen revealed that knockdown of genes involved in pausing
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control alters clock properties in U2OS cells (Zhang et al., 2009). Despite those indirect
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evidence, whether and how Pol II pausing is regulated have not been systematically studied
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(Takahashi, 2017). In this study, we performed ChIP-seq against Pol II to characterize Pol II
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pausing in the mouse liver. The results revealed widespread regulation of Pol II pausing and
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its complex relationship with transcription. We also performed Tbp ChIP-seq, and found that
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Pol II recruitment mainly plays an indirect role in determining transcriptional output, with its
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effect modulated by transcriptional termination and pause release.
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Materials and Methods:
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Animals. Young male C57BL/6 mice (3-4 months old) were housed in a 12:12 LD cycle with
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food and water freely available. Room temperature was maintained at 25 ºC. Mice were
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sacrificed by cervical dislocation, and livers were collected from 5 mice per time point and
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stored in liquid nitrogen. The time points were ZT2, 6, 10, 14, 18 and 22 (ZT: zeitgeber time.
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ZT0: lights on. ZT12: lights off). The study was approved by the Institutional Review Board
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of the College of Life Sciences, Wuhan University, and was conducted in accordance with
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internationally-accepted standards. 5
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Protein analysis. Nuclear proteins were extracted using the NUN method (Lavery and
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Schibler, 1993). Proteins not tightly associated with chromatin were released into the
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nucleoplasmic fraction, while those remained in the pellet (chromatin fraction) were isolated
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via sonication. For target detection by Western blot, proteins from the two compartments
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(with similar yields) were loaded in equal amounts. The primary antibodies used were: Cdk9
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(Santa Cruz, sc-484), NELF-A (Abcam, ab85852), NELF-E (Abcam, ab170104), Spt5 (CST,
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9033), and U2AF65 (Sigma, U4758). Quantitation result for each protein was shown as ratio
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against the mean on each gel.
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ChIP-seq. ChIP was performed according to (Nelson et al., 2006) with minor modifications.
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At each time point, frozen livers tissues from 5 mice were pooled by about equal weight and
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homogenized in 1% PFA (freshly prepared). After 10 minutes at RT, crosslinking was stopped
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via adding glycine to a final concentration of 125 mM. The nuclei were isolated via sucrose
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density gradient centrifugation, and sonicated in IP buffer (with 1% SDS). The sonicated
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chromatin was aliquotted and stored at -80 ºC. The same batch of chromatin prepared at each
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time point was used in all ChIPs. The ChIP antibodies were against Pol II (Santa Cruz: sc-899.
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Control: rabbit IgG) and Tbp (Abcam: ab51841. Control: mouse IgG). At each time point, 10
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µg chromatin and 2 µg antibody were used per ChIP, and 5 ChIPs were performed in parallel
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for each antibody. The IPed DNAs were pooled (to at least 10 ng). SE-50 ChIP-seq libraries
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were prepared at Beijing Genomics Institute at Shenzhen and sequenced on HiSeq 2000
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following standard protocols.
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ChIP-seq data analysis. Raw reads (tag size: 49 bps. Fastq format: Illumina 1.5+, Phred64
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quality score system) were subject to quality control as in (Patel and Jain, 2012). Reads
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passing the filtering criteria were aligned to the UCSC mm9 genome via Bowtie (v1.1.2)
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(Langmead et al., 2009). The –n mode was used with default settings, except that the –
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phred64-quals option was on. The first 28 bps of the read were used as the seed. At most 2
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mismatches in the seed region were allowed, and the sum of phred quality values at all
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mismatched positions of the entire read should not exceed 70. Reads with more than one
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mapping location were also discarded. The SAM alignment files were converted to BAM
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files via SAMtools (v1.3.1) (Li et al., 2009), sorted, and all duplicates were removed. The
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final BAM files only contained unique and non-redundant reads. We referred to the number
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of such reads as the sequencing depth of each sample. Genomic coverage of those reads was
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shown in Fig S1. Peak calling was performed via MACS (v1.4.2) (Feng et al., 2012). For
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model-based analysis, the fragment size estimates varied by ~10% among Pol II samples
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(average: 136 bp). To avoid bias in length estimate, we performed MACS analysis with a
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fixed tag shift of 68 bp (half of the average length estimate for Pol II samples) for all samples.
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The threshold p value for enrichment was set at 10-5. λlocal values were normalized to the IgG
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sample. The stats for read mapping and MACS analysis are in Table S1. The MACS peaks
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were not selected by FDR or fold enrichment. They were annotated with CEAS (Shin et al.,
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2009). For genomic average profiles, CEAS data at each time point were divided by a factor
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proportional to the sequencing depth at that time point (1 for sample with the lowest
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sequencing depth). For IGV display of bedgraph/wig files (Robinson et al., 2011), the data
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range was normalized by sequencing depth relative to that of IgG control. For example, IgG
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control had a depth of 20 million, while sample A had a depth of 15 million. If the data range
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in IGV was set at 100 for IgG, then the data range for sample A was set at 75 at the same
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height of data display. For overlap analysis, the UCSC mm9 refFlat list was downloaded.
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After removing annotation duplicates, the remaining 29933 genes were used in overlap
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analysis between MACS peaks and the TSS region via “intersect” of BEDTools (v.2.26.0)
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(Quinlan and Hall, 2010). At each time point, ~90% of overlapping events covered the entire
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TSS region. For the rest, the lengths of overlap did not cover the entire TSS region and/or
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changed over the day. All overlapping events were accepted without specifying the minimum
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overlap length.
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Quantitative binding analysis and Pol II TR calculation. Quantitative analysis of binding
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signals within TSS region and gene body and Pol II TR calculation were performed as in
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(Day et al., 2016) , with minor modifications. BAM files were processed by the R package
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SPP (v1.4) (Kharchenko et al., 2008), and all tags were selected. After removing local tag
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anomaly, a read extension of 136 bp was performed. Tag pileups within specified regions
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(TSS region and gene body) of target genes were normalized to region length and sequencing
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depth (read per bp per million). We used the definition of [-50, +300 bp] to TSS as the TSS
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region, and from +300bp downstream of TSS to annotated gene end as the gene body. A small
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fraction of Pol II signals within the TSS region ([Pol II]TSS) probably represented Pol II in the
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PIC and/or initiated Pol II before the establishment of pausing (Chen et al., 2015), although
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the exact proportion was difficult to determine based on our ChIP-seq data. We used [Pol
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II]TSS as a quantitative measure of paused Pol II in this study. For Tbp binding, defining the
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TSS region as [-80, +270 bp] to TSS, in accordance with the upstream location of Tbp peak
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relative to Pol II peak, resulted in [Tbp]TSS correlating well (~0.99 at ZT2) with original
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values. We used [-50, +300 bp] to TSS as the TSS region for all analyses. To determine
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whether Pol II signals could be corrected by IgG binding, we obtained tag counts within
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29933 refFlat genes’ boundaries (via Samtools -bedcov) and normalized them by sequencing
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depth. At each time point, there were more than 12000 genes whose Pol II coverage was
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lower than that of the IgG control. 11778 genes had more coverage in all Pol II samples than
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in IgG control. However, while most of those genes had TSS Pol II peaks, some clock genes
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(e.g. Arntl, Cry1, Per1, and Per3) with TSS Pol II peaks were excluded. Because the signals
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of the specific antibodies and IgG had time- and locus-specific variations in relative strength,
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IgG correction would reduce the number of genes with truly positive signals to be analyzed,
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including clock genes essential for our study. A simulated correction of [Pol II]TSS and [Pol
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II]GB by a fixed value (1.0E-6, close to the smallest [Pol II]GB value in our data) had almost
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no effect on rhythm analysis of TR. Alternatively, correction by dividing [Pol II]GB by a
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factor (e.g., 2) raised TR, without changing our conclusion either. All binding values
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presented were without correction. We prepared a list of more than 14000 genes harboring all
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TSS MACS peaks of Pol II and a protein involved in pausing control (done in parallel with
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Pol II ChIP-seq in a pilot study) over the day. This list covered more than 99% of the genes
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with TSS Tbp peaks. After removing transcript isoforms (typically the longest one was kept
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for each gene), overlapping genes, genes within 1 kb from each other, and genes shorter than
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1 kb, 7414 genes from this list were selected for quantitative analysis (Table S2-6). TR values
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in IgG control (less than 2 for ~40% of genes) were typically much smaller than those in Pol
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II samples.
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Rhythm analysis. Because our 1-cycle data could not be analyzed with JTK-CYCLE
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(Hughes et al., 2010), we used ARSER instead (Yang and Su, 2010). The cutoff p value was
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0.05 in all analyses. Overlap of genes rhythmic in different parameters was analyzed using
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Excel via functions such as sort and filter. ARSER analysis of 1-cycle [Tbp]TSS and [Pol
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II]TSS/[Tbp]TSS data resulted in misleading phase estimates that did not agree well with gross
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examination of heatmaps. Using 2-cycle data of duplication, as in (Koike et al., 2012), led to
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more appropriate phase estimate. It also resulted in more rhythmic genes in all parameters
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analyzed. The results on both 1-cycle and 2-cycle data were included in Table S2-6. For
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heatmaps, values were normalized by the daily mean of each gene, and genes were sorted by
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ARSER phase in ascending order.
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Data availability. Raw sequencing reads and bedgraph files produced by MACS (for IGV
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display) have been deposited into Gene Expression Omnibus (GSE96773).
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Results
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ChIP-seq Reveals Prominent Pol II binding near the TSS
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We set out to study Pol II pausing by characterizing Pol II distribution within the mouse liver
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genome via ChIP-seq at 6 time points across the day. The antibody is against the N-terminus
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of Rpb1 (the largest subunit of the Pol II complex), regardless of its CTD phosphorylation
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states. At each time point, ~14,000 to ~32,000 Pol II peaks were identified. About 20-40% of
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those peaks were within the promoter and 5’-UTR of genes (Fig S2). Such TSS-proximal
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peaks were evident in clock genes (Fig 1A). Genomic average profile also revealed a
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prominent Pol II peak near the TSS (Fig 1B), a pattern indicative of Pol II pausing. We
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defined the TSS region as from -50 to +300 bp relative to TSS (Fig 1B), following
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convention (Day et al., 2016). The TSS region did not cover the entire Pol II peak near the
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TSS. Pol II signals upstream of the TSS could arose from divergent transcription (i.e., a Pol II
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peak upstream of the TSS) (Almada et al., 2013). To our benefit, the TSS region thus defined
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typically excluded such upstream Pol II signals when examined with IGV. The relatively high
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Pol II signals downstream of the TSS region (up to 1 kb into the gene body) most probably
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reflected increased Pol II density due to the low speed of Pol II elongation just after pause
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release (Jonkers et al., 2014). At each time point, ~30-56% of the Pol II MACS peaks had
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overlap with the defined TSS region of genes (Fig. 1C). About 99% of genes with TSS Pol II
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peaks at other time points also had such peaks at ZT2, when the greatest numbers of such
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genes were found (Fig 1D). The daily changes in the number of genes with TSS Pol II peaks
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indicated that Pol II signals near the TSS changed over the day, warranting quantitative
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analysis. About 10-15% of the Pol II peaks were within intergenic regions (Fig S2), probably
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occupying enhancers (Kim et al., 2010). They were not further analyzed. Despite the
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relatively low Pol II average profile within the gene body, ~40-50% of Pol II MACS peaks
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were found within coding exons and introns at each time point (Fig S2). While we did not
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analyze those peaks either, average Pol II binding within gene body could be used as a
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measure of transcription (Le Martelot et al., 2012), allowing a quantitative study of gene
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transcription via ChIP-seq.
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Quantitative Analysis of Pol II binding Reveal Distinct Pol II binding within the TSS
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Region and Gene Body
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To study the relationship between TSS Pol II binding and transcription within the gene body,
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we quantitated Pol II signals within the TSS region ([Pol II]TSS) and gene body ([Pol II]GB)
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for 7414 genes across the genome. The values (without background subtraction) were
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normalized to sequencing depth and region length. We found that [Pol II]GB, but not [Pol
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II]TSS always, reflected temporal changes in the transcription of genes (Fig 2). Genes such as
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Bmal1, Fgf21, and Gys2 had nearly synchronized changes in their [Pol II]TSS and [Pol II]GB.
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However, for genes such as Cry2, Nampt, and Per3, their daily [Pol II]TSS and [Pol II]GB
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profiles were dramatically different, with the latter conforming to their known expression
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patterns (Fig 2). These observations validated the approach of using [Pol II]GB as a measure
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of transcription level, and indicated that [Pol II]GB was not always passively determined by
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[Pol II]TSS. To further study such dissociation, we performed rhythm analysis of [Pol II]TSS
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and [Pol II]GB. For 2535 genes rhythmic in [Pol II]TSS (Table S2), the phases were clustered
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around ZT0 (Fig 3A), a pattern also evident in all genes (Fig S1B&S3). Consistent with this
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finding, pSer5-CTD, a marker of paused Pol II, was previously shown to exhibit daily
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changes that peaked similarly near CT0 (Koike et al., 2012). Those results supported the
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notion that TSS Pol II peaks represent paused Pol II, and indicated that there was a global
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rhythm of Pol II pausing. 665 genes were identified as rhythmic in [Pol II]GB, but their phases
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had a bimodal distribution (Fig 3C). A prominent [Pol II]GB peak cluster of ~400 genes
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(including ~60 genes coding for transcription factors, histone modification enzymes, and
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mediators) was found near ZT0, when the [Pol II]TSS rhythms also peaked. However, another
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peak cluster of ~300 genes was found near ZT12 (Fig 3C), in anti-phase to the [Pol II]TSS
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rhythm (Fig 3D). Because 1-cycle data of low sampling resolution (4-hr interval) were
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analyzed, the number of rhythmic genes was likely an underestimate, and few clock genes
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were identified as rhythmic in [Pol II]GB (Table S3). Loosening the detection criteria by
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analyzing 2-cycle data of duplication resulted in more genes rhythmic in transcription,
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including those whose transcription peaked at times beyond near ZT0 and ZT12 (Table S3).
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However, the bimodal pattern was independent of detection criteria and evident even when
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all genes were considered as rhythmic (Fig S4). Thus, our results were not biased. However,
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despite the transcriptional peak cluster near ZT12, our pan-Pol II antibody did not reveal a
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rise of [Pol II]TSS at that time (Fig S3), in contrast to previous result with the 8WG16
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antibody (Koike et al., 2012). The reason for such discrepancy is not clear, but the
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cross-reactivity of Pol II CTD antibodies (e.g., 8WG16) to various pCTD forms could
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confound ChIP-seq results (Nojima et al., 2015).
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Pol II Pausing is Related to Transcription in Complex Ways
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The discordant changes of [Pol II]TSS and [Pol II]GB across the day prompted us to calculate
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Pol II traveling ratio (TR: [Pol II]TSS/[Pol II]GB, a.k.a. the pausing index), a quantitative
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measure of Pol II pausing (Rahl et al., 2010;
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II elongation complex is known to gain speed when transcribing into gene body (Jonkers et
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al., 2014). Accordingly, more Pol II is expected to travel at maximum speed in the gene
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bodies of longer genes, potentially leading to lower Pol II density therein, hence higher TR.
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There was indeed a positive correlation between TR and gene length (Fig S9). However, such
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correlation was weak. Pol II elongation kinetics also varies across genes (Jonkers et al., 2014).
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In this study, we assumed that the overall kinetics of Pol II elongation does not change over
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the day for each gene. TR values had a broad distribution (Fig 4A, left), and exhibited daily
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changes by more than 1.5 fold for ~95% of genes (Table S4). At each time point, ~90% of
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genes had TR larger than 2 (Fig 4A, right). Nearly all genes had TR larger than 2 at least at
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one time point (Table S4). Interestingly, TR curves for ZT2, ZT6, and ZT10 were similar to
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Day et al., 2016). After pause release, the Pol
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those for ZT22, ZT18, and ZT14, respectively, resulting in a near symmetrical pattern across
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the day (Fig 4A, right). Overall, TR was smaller at ZT10 and ZT14, but higher at ZT2 and
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ZT22 (Fig 4A). For 2123 genes rhythmic in TR, their phases were clustered near ZT0 (Fig
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4B&S6), similar to the [Pol II]TSS rhythm (Fig 3A). For 1463 genes rhythmic in both [Pol
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II]TSS and TR (Fig 4C), the phases of the two rhythms agreed well (with only 2 exceptions.
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Fig 4D). In contrast, for genes rhythmic in both TR and [Pol II]GB, a bimodal pattern of
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association was evident. There were genes whose transcription peaked near ZT12, in
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anti-phase to the [Pol II]TSS and TR rhythms (Fig 3&4D). A rise of pause release, to decrease
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pausing and increase elongation, could potentially account for increased transcription of these
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genes near ZT12. The expression of proteins involved in pausing control (Fig S8), however,
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did not have a clear relationship with the global rhythm of Pol II pausing. ChIP-seq studies
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on those proteins’ DNA association are needed to characterize whether and how pause release
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activity varies over the day for specific genes. On the other hand, [Pol II]TSS represents net
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accumulation of Pol II within the TSS region, where initiated Pol II can be removed via not
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only pause release but also premature termination (Jonkers and Lis, 2015). A reduction in
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[Pol II]TSS and TR does not necessarily reflect an increase in pause release activity, but could
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be due to increased transcriptional termination as well. Such caution is warranted, given the
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near symmetrical distribution of TR and [Pol II]TSS values across the day for most genes (Fig
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S3&6). These patterns reflected complex interactions between transcriptional termination and
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pause release after Pol II initiation. Further arguing against pause release as the sole
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determinant of transcription level and TR, there were a few genes whose TRs peaked near
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ZT12, but their transcription peaked near ZT0 (Fig 4D). Moreover, there were genes whose
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transcription and TR both peaked near ZT0 (Fig 4D), when [Pol II]TSS also peaked (Fig 3D),
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presumably due to low pause release activity. For these genes, more Pol II initiation was
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required to increase [Pol II]TSS, [Pol II]GB, and TR at the same time. The results thus agreed
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with a role of Pol II initiation in driving transcription, as suggested previously (Le Martelot et
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al., 2012). On the other hand, from the perspective of Pol II pausing, the results were also
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consistent with a positive role of Pol II pausing in transcription, as revealed in previous
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studies (Gilchrist et al., 2010;
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always a positive correlation between [Pol II]GB and [Pol II]TSS across genes (Fig S7).
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However, within-gene correlation between [Pol II]TSS and [Pol II]GB across the 6 time points
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were highly variable, with poor or negative correlation being frequent (Fig 4E). Overall, [Pol
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II]TSS was not always a good predictor of [Pol II]GB. Thus, despite the global rhythm of Pol II
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pausing, the temporal output of transcription was mostly regulated in a gene-specific manner.
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This was due to the complexity of transcriptional control, which occurs at three levels near
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the TSS: Pol II recruitment and initiation, transcriptional termination, and pause release.
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The Effect of Pol II Recruitment and Initiation to Transcription is Modulated by
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Transcriptional Termination and Pause Release
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To study the role of Pol II recruitment and initiation in daily transcription, we performed
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ChIP-seq against the PIC component Tbp (TATA-binding protein). Tbp signals near the TSS
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of Cry2 and Per1 appeared relatively weak, especially when compared to strong signals at the
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3’-end of the Per1 gene (Fig 5A&S9A). Nonetheless, MACS analysis revealed that Tbp
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peaks were mainly located near the TSS (Fig S10). Genomic average profiles revealed a Tbp
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peak slightly upstream of the TSS (Fig 5B&S9B), with a much lower peak height than that of
Nilson et al., 2015). Indeed, at each time point, there was
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Poll (Fig S9C). Across the day, most numbers of Tbp peaks (genomewide or within the TSS
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region) were found at ZT2 (Fig 5C). Most of the genes with TSS Tbp peaks at other time
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points were also found at ZT2 (Fig 5D). Overall, the TSS Tbp peaks were found within
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nearly the same set of genes that also had TSS Pol II peaks (Fig 5E & S9D). Those results
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were consistent with Tbp being a PIC component, while the TSS Pol II peak represents
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mainly paused Pol II after initiation. 269 genes were rhythmic in [Tbp]TSS (Fig 6A), which
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had marginal overlap with those rhythmic in [Pol II]TSS or [Pol II]GB (Fig 6B). The number of
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genes rhythmic in [Tbp]TSS appeared greatly underestimated, since heatmap revealed a
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genomewide trend of decreasing [Tbp]TSS values over the day, peaking at ZT2 for most genes
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(Fig S11). Such peculiar waveforms, far from symmetrical, could have hindered rhythm
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detection. We also noticed that [Tbp]TSS phase values based on 1-cycle data analysis differed
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from those based on 2-cycle data, with the latter closer to intuitive estimates according to
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heatmap (Fig S11). We thus did not analyze the phase relationship between [Tbp]TSS and [Pol
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II]TSS (or [Pol II]GB). Genomewide, there was a positive correlation between [Tbp]TSS and
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[Pol II]TSS across genes at each time point (Fig S12A). However, within-gene correlation
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between [Tbp]TSS and [Pol II]TSS (or [Pol II]GB) across the day was highly variable, with poor
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correlation being frequent (Fig 6C&D. Fig S12B for examples). Such results indicate that Pol
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II recruitment is not the direct determinant of Pol II pausing or transcriptional output on most
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occasions. This is due to the fact that both premature termination and pause release reduce
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[Pol II]TSS, but with opposite effects on [Pol II]GB. Assuming that [Tbp]TSS is a quantitative
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measure of Pol II recruitment and Pol II initiation is efficient, the [Pol II]TSS/[Tbp]TSS ratio
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can be used as a stability index of initiated Pol II. Analysis of this index showed that initiated
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Pol II was more stable at ZT22, with intermediate stability at ZT14, but much less stable at
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ZT2/10 (Fig 6E), a pattern also evident in genes rhythmic in this index (Fig 6F&S13).
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Because Pol II TR was high at ZT2/22, but low at ZT10/14, there is no clear temporal
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association between TR and Pol II stability. Thus, a complex interplay between pause release
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and trancriptional termination determines the fate of initiated Pol II and its pausing status.
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Discussion
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In this study, we showed that Pol II pausing control is involved in transcription in the mouse
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liver. The results provided clear evidence for separate regulation of [Pol II]TSS and [Pol II]GB,
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and revealed global changes in Pol II TR. Our results indicate that both pause release and
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transcriptional termination are involved in the regulation of Pol II pausing. They modulate the
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effect of Pol II recruitment, and shape the temporal profiles of transcription in a gene-specific
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manner. Our results were based on 1-cycle data of low sampling resolution, thus statistically
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underpowered (Hughes et al., 2017). Additional biological replicates and/or higher sampling
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resolution are required to characterize Pol II pausing more rigorously. Nonetheless, some
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insights could still be gained from our study.
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The global decrease in [Pol II]TSS and Pol II TR near ZT12 (especially at ZT14) is probably
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due to an increase in pause release activity at that time. Evidence in literature supports such a
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scenario. During pause release, P-TEFb promotes the recruitment of PAF1 complex (Yu et al.,
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2015), which in turn recruits histone modifying enzymes (e.g., for H2B ubiquitination and
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H3K4 methylation) and the chromatin remodeler Chd1 (for +1 nucleosome turnover) 17
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(Tomson and Arndt, 2013). The level of tri-methyl H3K4, a marker of transcription near TSS,
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peaked near CT14 (Koike et al., 2012). The level of H2A.Z, another transcription mark near
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TSS, also peaked at ZT14, distinct from the ZT6 peak due to maximal BMAL1 binding
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(Menet et al., 2014). Those results are consistent with a daily rise of Pol II pause release
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activity near dusk, when ~300 genes reached peak transcription according to our data. On the
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other hand, previous studies suggested that Pol II pausing has a positive role in transcription
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by keeping an open chromatin state near the TSS (Gilchrist et al., 2010; Nilson et al., 2015).
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Indeed, our results revealed that the transcription of ~400 genes peaked near ZT0, when
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pause release activity was presumably low. For these genes, greater TSS Pol II accumulation
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appeared sufficient to increase their transcription. There were probably other genes whose
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transcription peaked at times beyond near ZT0 and ZT12. Thus, Pol II pausing status is
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temporally related to transcription in a gene-specific manner. Factors other than pause release
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must be involved in determining such relationships. One candidate is Pol II initiation.
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However, our results showed that within-gene correlation between [Tbp]TSS and [Pol II]GB
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over the day was gene-specific, ruling out Pol II initiation as the direct determinant of
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transcription output for a majority of genes. We conclude that transcription is determined in a
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mostly gene-specific manner, owing to the interplay among 3 factors: Pol II initiation,
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transcriptional termination (regulating the fraction of initiated Pol II available for pause
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release), and pause release (controlling the fraction of available Pol II for release into
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elongation). The 3 factors could act at genes with distinct temporal characteristics, resulting
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in gene-specific transcription output. The interplay between transcriptional termination and
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pause release modulates the effect of Pol II recruitment to transcription, and determine the
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stability of initiated Pol II. ChIP-seq against pause release markers and transcriptional
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terminators is required to study the daily changes in premature termination and pause release
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at the 5’-end of genes. Inhibitors can be used to differentiate the roles of Pol II initiation and
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pause release in transcription. While pause release is blocked by the Cdk9 inhibitor DRB
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(Chodosh et al., 1989), Pol II initiation is inhibited by triptolide (Titov et al., 2011). The
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effects of DRB and triptolide on transcription and clock oscillation should be compared.
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While we focused mainly on Tbp and Pol II signals near the TSS and/or within gene body,
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previous studies also revealed daily changes in enhancer activity (Koike et al., 2012; Fang
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et al., 2014). Enhancers are known to influence transcription through eRNA production and
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pause release (Kim et al., 2010; Liu et al., 2013; Schaukowitch et al., 2014). Thus, the
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interactions among the clock, enhancers, and core promoters ultimately regulate transcription
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through Pol II pausing control. In this regard, the global rhythm of Pol II pausing we revealed
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is intriguing and provides new perspectives of circadian rhythm generation. The contribution
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of pausing regulation to circadian transcription should be studied in mice bearing mutations
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of relevant genes. The role of the clock in Pol II pausing also needs to be characterized.
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Another question is how feeding, a potent regulator of gene expression in peripheral tissues
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(Damiola et al., 2000), is involved in Pol II pausing regulation. Given the clock-independent
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rhythm of mTOR activation in livers of fasted mice (Khapre et al., 2014), however, it is
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probably difficult to completely dissect the role of feeding in Pol II pausing regulation. It is
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possible that the temporal regulation of Pol II pausing in the mouse liver is an emergent
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feature due to the integration of clock and metabolism.
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Acknowledgements. The authors thank BGI-Shenzhen for preparing and sequencing
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ChIP-seq libraries. The authors are grateful to Prof. William Pu (Children’s Hospital Boston)
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and Dr. Daniel Day (MIT) for sharing the Pol II TR script, and Prof. Michael E. Hughes
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(Washington University at St. Louis) for sharing the JTK_CYCLE script. Prof. Frederick
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Davis (Northeastern University, Boston) provided valuable comments to the manuscript. Part
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of the numberical calculations in this paper were done on the supercomputing system in the
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Supercomputing Center of Wuhan University.
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The authors declare that there is no conflict of interest.
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Robinson JT, Thorvaldsdottir H, Winckler W, Guttman M, Lander ES, Getz G, and Mesirov JP (2011) Integrative genomics viewer. Nat Biotechnol 29:24-26. Schaukowitch K, Joo JY, Liu X, Watts JK, Martinez C, and Kim TK (2014) Enhancer RNA facilitates NELF release from immediate early genes. Mol Cell 56:29-42. Shin H, Liu T, Manrai AK, and Liu XS (2009) CEAS: cis-regulatory element annotation system. Bioinformatics 25:2605-2606. Skene PJ, Hernandez AE, Groudine M, and Henikoff S (2014) The nucleosomal barrier to promoter escape by RNA polymerase II is overcome by the chromatin remodeler Chd1. Elife 3:e02042. Takahashi JS (2017) Transcriptional architecture of the mammalian circadian clock. Nat Rev Genet 18:164-179. Titov DV, Gilman B, He QL, Bhat S, Low WK, Dang Y, Smeaton M, Demain AL, Miller PS, Kugel JF, Goodrich JA, and Liu JO (2011) XPB, a subunit of TFIIH, is a target of the natural product triptolide. Nat Chem Biol 7:182-188. Tomson BN, and Arndt KM (2013) The many roles of the conserved eukaryotic Paf1 complex in regulating transcription, histone modifications, and disease states. Biochim Biophys Acta 1829:116-126. Weber CM, Ramachandran S, and Henikoff S (2014) Nucleosomes are context-specific, H2A.Z-modulated barriers to RNA polymerase. Mol Cell 53:819-830. Yamaguchi Y, Shibata H, and Handa H (2013) Transcription elongation factors DSIF and NELF:
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Yu M, Yang W, Ni T, Tang Z, Nakadai T, Zhu J, and Roeder RG (2015) RNA polymerase II-associated factor 1 regulates the release and phosphorylation of paused RNA polymerase II. Science 350:1383-1386. Zhang EE, Liu AC, Hirota T, Miraglia LJ, Welch G, Pongsawakul PY, Liu X, Atwood A, Huss JW, 3rd, Janes J,
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Zhang T, Kwiatkowski N, Olson CM, Dixon-Clarke SE, Abraham BJ, Greifenberg AK, Ficarro SB, Elkins JM, Liang Y, Hannett NM, Manz T, Hao M, Bartkowiak B, Greenleaf AL, Marto JA, Geyer M, Bullock AN, Young RA, and Gray NS (2016) Covalent targeting of remote cysteine residues to develop CDK12 and CDK13 inhibitors. Nat Chem Biol 12:876-884.
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Figure legends
573
Fig 1. Pol II ChIP-seq. (A) Examples of Pol II ChIP-seq results. IGV display of Cry2 and
574
Per1 results. Data range is normalized by sequencing depth to that of IgG (set to 120). (B)
575
TSS-centered (± 3 kb) genome-wide average Pol II profile. Data (produced by CEAS) are
576
scaled according to sequencing depth relative to sample with the lowest depth. The TSS
577
region, defined as [-50 bp, 300 bp] to TSS, is also shown. The three dashed lines cross the 23
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x-axis at -50 bp, 0 bp, and 300 bp relative to TSS, respectively. (C) Summary of Pol II peaks.
579
The MACS peaks are grouped as either within the TSS region or not, and their numbers are
580
shown. If a MACS peak is shared by genes due to their proximity, only one peak is counted.
581
(D) Venn diagram showing overlap among genes with TSS Pol II peaks across the day. Most
582
genes with TSS Pol II peaks at other time points are also found at ZT2. Overlapping
583
(including isoforms) and neighboring genes that share TSS Pol II peaks are all counted. If a
584
gene has multiple TSS Pol II peaks, only one gene is counted.
585
Fig 2. [Pol II]GB and [Pol II]GB show discordant changes for certain genes. Within-gene
586
correlation value (between [Pol II]TSS and [Pol II]GB across 6 time points) is shown for each
587
gene. The temporal changes in [Pol II]GB better reflect the known expression patterns of
588
genes. (A) [Pol II]TSS (red, left y-axis. Unit: read per million per bp) and [Pol II]GB (blue,
589
right y-axis) change in close parallel for Arntl, Fgf21, Gys2, Npas2, Per1, and Tef. (B)
590
Discordant changes are found for Alas1, Bnip3, Cry2, Nampt, Per3 and Pparγ.
591
Fig 3. Rhythm analysis of [Pol II]TSS and [Pol II]GB. Mean-normalized values are displayed
592
in heatmaps, where genes are sorted by ARSER phase in ascending order. (A) [Pol II]TSS
593
rhythms. Upper: heatmap. Lower: histogram of phase distribution (0.5 hr bin). (B) [Pol II]GB
594
rhythms. Upper: heatmap. Lower: histogram of phase distribution. 271 genes are rhythmic in
595
both [Pol II]TSS and [Pol II]GB (C), and the respective phases of [Pol II]TSS and [Pol II]GB are
596
plotted as x-y scatter (D).
597
Fig 4. Daily changes in Pol II traveling ratio. (A) TR distribution. Left: daily average TR
598
values of genes (in red. N = 7414) are ranked and plotted against cumulative distribution.
599
Blue error bars represent standard deviations over the 6 time points. Right: TR values at each
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time point are ranked and plotted against cumulative distribution. Note that values at ZT10
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and ZT14 are smaller (left-shifted). The curves of ZT2 and ZT22 (and ZT6/18) appear nearly
602
indistinguishable. (B) TR rhythms. Left: heatmap. Right: histogram of phase distribution. (C)
603
Venn diagram showing overlap among genes rhythmic in TR, [Pol II]TSS, or [Pol II]GB. (D)
604
For genes rhythmic in both TR and [Pol II]TSS (left. n = 1463), or rhythmic in both TR and
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[Pol II]GB (right. n = 194), the respective phases are plotted as x-y scatter. (E) Within-gene
606
correlation between [Pol II]TSS and [Pol II]GB across 6 time points. Note that many genes have
607
poor or negative correlation.
608
Fig 5. Tbp ChIP-seq results. (A) Tbp ChIP-seq results for the Cry2 and Per1 gene. Note the
609
strong Tbp signals at the 3’-end of Per1. (B) TSS-centered (± 3kb) average Tbp binding
610
profile. Data are normalized relative to the sample with the lowest sequencing depth. The Tbp
611
peak is located slightly upstream of the TSS. (C) Overlap between the Tbp MACS peaks and
612
the TSS region of genes. The Tbp peaks are classified as either overlapping with the TSS
613
region or not. The numbers of such peaks at each time point are shown. (D) Venn diagram
614
showing overlap among genes with TSS Tbp peaks at each of the 6 time points. Most genes
615
with TSS Tbp peaks at other time points can be found at ZT2. (E) Overlap between genes
616
with TSS Pol II and Tbp peaks. The numbers of genes with both TSS Pol II and TSS Tbp
617
peaks, TSS Pol II peaks only, or TSS Tbp peaks only are shown for each time point.
618
Fig 6. Indirect contribution of Pol II recruitment to transcriptional rhythms. (A)
619
Analysis of the [Tbp]TSS rhythms. Left: heatmap for 269 genes rhythmic in [Tbp]TSS. (B)
620
Venn diagram showing overlap among genes rhythmic in [Tbp]TSS, [Pol II]TSS, or [Pol II]GB.
621
(C) Within-gene correlation between [Tbp]TSS and [Pol II]TSS across the 6 time points. (D)
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Journal of Biological Rhythms
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Within-gene correlation between [Tbp]TSS and [Pol II]GB across the 6 time points. (E) Daily
623
changes in Pol II stability. The [Pol II]TSS/[Tbp]TSS ratios for 7414 genes are ranked at each
624
time point and plotted against cumulative distribution. In general, values are larger at ZT22,
625
intermediate at ZT14, and smaller at ZT2 and ZT10. (F) Heatmap for 617 genes rhythmic in
626
[Pol II]TSS/[Tbp]TSS. For most of those genes, higher stability is found at ZT18 and ZT22, a
627
pattern also evident in all genes (Fig S13).
628
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629
Supplementary material
630
Figure S1. Antibody coverage analysis. (A) Fractions of reads (uniquely mapped without
631
duplicates) aligned to specific genomic regions (TSS region: -50 to 300 bp to TSS; Gene:
632
TSS to TTS) are shown for antibody against Pol II, Tbp, and IgGs. (B) Daily changes in [Pol
633
II]TSS, [Pol II]GB and [Tbp]TSS. At each time point, [Pol II]TSS, [Pol II]GB and [Tbp]TSS values
634
of the 7414 genes selected for quantitative analysis are ranked and plotted against cumulative
635
distribution. Note the broad but near symmetrical distribution of [Pol II]TSS curves of the 6
636
time points, with values similarly low at ZT10 and ZT14. [Pol II]GB curves are intermingled
637
within a relatively narrow range. [Tbp]TSS curves have a broad distribution, but without a
638
symmetrical pattern. Unit of value: RPBM (read per bp per million).
639
Figure S2. Annotation of Pol II MACS peaks.
640
Figure S3. ARSER analysis of [Pol II]TSS. Results based on both 1-cycle and 2-cycle data
641
are compared. (A) Heatmap. The 7414 genes are sorted by phase in ascending order. (B)
642
Histogram of phase distribution. (C) Scatter plot of respective phase values obtained from
643
1-cycle and 2-cycle data.
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644
Figure S4. ARSER analysis of [Pol II]GB. Results based on both 1-cycle and 2-cycle data are
645
compared. (A) Heatmap. The 7414 genes are sorted by phase in ascending order. (B)
646
Histogram of phase distribution. A bimodal pattern is evident. (C) Scatter plot of respective
647
phase values obtained from 1-cycle and 2-cycle data.
648
Figure S5. Correlation between TR and gene length. Across-gene correlation between TR
649
and gene length is shown. There is a positive but weak correlation at each time point. All
650
correlations are statistically significant (p < 0.01).
651
Figure S6. ARSER analysis of TR. Results based on 1-cycle and 2-cycle data are compared.
652
(A) Heatmap. The 7414 genes are sorted by phase in ascending order. (B) Histogram of phase
653
distribution. (C) Scatter plot of respective phase values based on 1-cycle and 2-cycle data.
654
Figure S7. Correlation between [Pol II]GB and [Pol II]TSS. Across-gene correlation between
655
[Pol II]GB and [Pol II]TSS at each time point. All correlations are significant (p 3 * , # / . , 3 #
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Journal of Biological Rhythms
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Journal of Biological Rhythms
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Journal of Biological Rhythms
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Journal of Biological Rhythms
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Journal of Biological Rhythms
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