Diurnal RNAPII-tethered chromatin interactions are associated with rhythmic gene expression in rice

Abstract Background The daily cycling of plant physiological processes is speculated to arise from the coordinated rhythms of gene expression. However, the dynamics of diurnal 3D genome architecture and their potential functions underlying the rhythmic gene expression remain unclear. Results Here, we reveal the genome-wide rhythmic occupancy of RNA polymerase II (RNAPII), which precedes mRNA accumulation by approximately 2 h. Rhythmic RNAPII binding dynamically correlates with RNAPII-mediated chromatin architecture remodeling at the genomic level of chromatin interactions, spatial clusters, and chromatin connectivity maps, which are associated with the circadian rhythm of gene expression. Rhythmically expressed genes within the same peak phases of expression are preferentially tethered by RNAPII for coordinated transcription. RNAPII-associated chromatin spatial clusters (CSCs) show high plasticity during the circadian cycle, and rhythmically expressed genes in the morning phase and non-rhythmically expressed genes in the evening phase tend to be enriched in RNAPII-associated CSCs to orchestrate expression. Core circadian clock genes are associated with RNAPII-mediated highly connected chromatin connectivity networks in the morning in contrast to the scattered, sporadic spatial chromatin connectivity in the evening; this indicates that they are transcribed within physical proximity to each other during the AM circadian window and are located in discrete “transcriptional factory” foci in the evening, linking chromatin architecture to coordinated transcription outputs. Conclusion Our findings uncover fundamental diurnal genome folding principles in plants and reveal a distinct higher-order chromosome organization that is crucial for coordinating diurnal dynamics of transcriptional regulation.

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The largest subunit of RNA polymerase II in Dictyostelium: conservation of the unique tail domain and gene expression

Biochemistry and Cell Biology ◽

10.1139/o92-120 ◽

1992 ◽

Vol 70 (9) ◽

pp. 792-799 ◽

Cited By ~ 4

Author(s):

Tak Yee Lam ◽

Lawrence Chan ◽

Patrick Yip ◽

Chi-Hung Siu

Keyword(s):

Gene Expression ◽

Rna Polymerase ◽

Rna Polymerase Ii ◽

Developmental Process ◽

Developmental Regulation ◽

Consensus Sequence ◽

Protein Band ◽

Tail Domain ◽

Mrna Accumulation ◽

Carboxyl Terminal

cDNAs encoding the largest subunit of RNA polymerase II were isolated from a Dictyostelium cDNA library. A total of 2.9 kilobases (kb) of cDNA was sequenced and the amino acid sequence of the carboxyl-terminal half of the protein was deduced. Similar to other eukaryotic RNA polymerases II, the largest subunit of Dictyostelium RNA polymerase II contains a unique repetitive tail domain at its carboxyl-terminal region. It consists of 24 highly conserved heptapeptide repeats, with a consensus sequence of Tyr-Ser-Pro-Thr-Ser-Pro-Ser. In addition to the tail domain, five segments of the deduced primary structure show > 50% sequence identity with either yeast or mouse protein. RNA blots show that cDNA probes hybridized with a single mRNA species of ~ 6 kb and immunoblots using a monoclonal antibody raised against the tail domain lighted up a single protein band of 200 kilodaltons. Interestingly, expression of the largest subunit of RNA polymerase II appears to be under developmental regulation. The accumulation of its mRNA showed a 60% increase during the first 3 h of development, followed by a steady decrease during the next 6 h. Cells began to accumulate a higher level of the RNA polymerase II mRNA after 9 h of development. When cells were treated with low concentrations of cAMP pulses to stimulate the developmental process, the pattern of mRNA accumulation moved 3 h ahead, but otherwise remained similar to that of control cells.Key words: RNA polymerase, cDNA, sequence homology, gene expression, Dictyostelium.

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Generation and timing of graded responses to morphogen gradients

Development ◽

10.1242/dev.199991 ◽

2021 ◽

Vol 148 (24) ◽

Author(s):

Shari Carmon ◽

Felix Jonas ◽

Naama Barkai ◽

Eyal D. Schejter ◽

Ben-Zion Shilo

Keyword(s):

Gene Expression ◽

Rna Polymerase Ii ◽

Target Genes ◽

Cell Formation ◽

Embryonic Cell ◽

Mrna Accumulation ◽

Temporal Regulation ◽

Morphogen Gradients ◽

Graded Response ◽

Spatio Temporal

ABSTRACT Morphogen gradients are known to subdivide a naive cell field into distinct zones of gene expression. Here, we examine whether morphogens can also induce a graded response within such domains. To this end, we explore the role of the Dorsal protein nuclear gradient along the dorsoventral axis in defining the graded pattern of actomyosin constriction that initiates gastrulation in early Drosophila embryos. Two complementary mechanisms for graded accumulation of mRNAs of crucial zygotic Dorsal target genes were identified. First, activation of target-gene expression expands over time from the ventral-most region of high nuclear Dorsal to lateral regions, where the levels are lower, as a result of a Dorsal-dependent activation probability of transcription sites. Thus, sites that are activated earlier will exhibit more mRNA accumulation. Second, once the sites are activated, the rate of RNA Polymerase II loading is also dependent on Dorsal levels. Morphological restrictions require that translation of the graded mRNA be delayed until completion of embryonic cell formation. Such timing is achieved by large introns, which provide a delay in production of the mature mRNAs. Spatio-temporal regulation of key zygotic genes therefore shapes the pattern of gastrulation.

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Transcription through the eye of a needle: daily and annual cycles of gene expression variation in Douglas-fir needles

10.1101/117374 ◽

2017 ◽

Cited By ~ 3

Author(s):

Richard Cronn ◽

Peter C. Dolan ◽

Sanjuro Jogdeo ◽

Jill L. Wegrzyn ◽

David B. Neale ◽

...

Keyword(s):

Gene Expression ◽

De Novo ◽

Clock Genes ◽

Rank Order ◽

Douglas Fir ◽

Mrna Accumulation ◽

Annual Cycles ◽

Plant Genomes ◽

Annual Peak ◽

Maximum Expression

BackgroundPerennial growth in plants is the product of interdependent cycles of daily and annual stimuli that induce cycles of growth and dormancy. In conifers, needles are the key perennial organ that integrates daily and seasonal signals from light, temperature, and water availability. To understand the relationship between seasonal rhythms and seasonal gene expression responses in conifers, we examined diurnal and circannual needle mRNA accumulation in Douglas-fir (Pseudotsuga menziesii) needles at diurnal and circannual scales. Using mRNA sequencing, we sampled 6.1×109 microreads from 19 trees and constructed a de novo pan-transcriptome reference that includes 173,882 tree-derived transcripts. Using this reference, we mapped RNA-Seq reads from 179 samples that capture daily, seasonal, and annual variation.ResultsWe identified 12,042 diurnally-cyclic transcripts, 9,299 of which showed homology to annotated genes from other plant genomes, including angiosperm core clock genes. Annual analysis revealed 21,225 an-nually-cyclic transcripts, 17,335 of which showed homology to annotated genes from other plant genomes. The timing of maximum gene expression is associated with light quality at diurnal and photoperiod at annual scales, with two-thirds of transcripts reaching maximum expression +/− 2 hours from sunrise and sunset, and half reaching maximum expression +/− 20 days from winter and summer solstices. Comparison to published microarray-based gene expression studies in spruce (Picea) show that the rank order of expression for 760 putatively orthologous genes was significantly preserved, highlighting the generality of our findings.ConclusionsThis finding highlights the extensive annual and seasonal transcriptome variability demonstrated in conifer needles. At these temporal scales, 29% of expressed transcripts showed a significant diurnal rhythm, and 58.7% showed a significant circannual rhythm. Remarkably, thousands of genes reach their annual peak activity during winter dormancy, a time of metabolic stasis. Photoperiod appears to be a dominant driver of annual transcription patterns in Douglas-fir, and these results may be general for predicting rhythmic transcription patterns in emerging gymnosperm models.

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Circadian and feeding rhythms differentially affect rhythmic mRNA transcription and translation in mouse liver

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1515308112 ◽

2015 ◽

Vol 112 (47) ◽

pp. E6579-E6588 ◽

Cited By ~ 121

Author(s):

Florian Atger ◽

Cédric Gobet ◽

Julien Marquis ◽

Eva Martin ◽

Jingkui Wang ◽

...

Keyword(s):

Gene Expression ◽

Circadian Clock ◽

Mouse Liver ◽

Mitochondrial Activity ◽

Translation Efficiency ◽

Mrna Transcription ◽

Mrna Accumulation ◽

Feeding Rhythms ◽

Rhythmic Gene ◽

Living Organisms

Diurnal oscillations of gene expression are a hallmark of rhythmic physiology across most living organisms. Such oscillations are controlled by the interplay between the circadian clock and feeding rhythms. Although rhythmic mRNA accumulation has been extensively studied, comparatively less is known about their transcription and translation. Here, we quantified simultaneously temporal transcription, accumulation, and translation of mouse liver mRNAs under physiological light–dark conditions and ad libitum or night-restricted feeding in WT and brain and muscle Arnt-like 1 (Bmal1)-deficient animals. We found that rhythmic transcription predominantly drives rhythmic mRNA accumulation and translation for a majority of genes. Comparison of wild-type and Bmal1 KO mice shows that circadian clock and feeding rhythms have broad impact on rhythmic gene expression, Bmal1 deletion affecting surprisingly both transcriptional and posttranscriptional levels. Translation efficiency is differentially regulated during the diurnal cycle for genes with 5′-Terminal Oligo Pyrimidine tract (5′-TOP) sequences and for genes involved in mitochondrial activity, many harboring a Translation Initiator of Short 5′-UTR (TISU) motif. The increased translation efficiency of 5′-TOP and TISU genes is mainly driven by feeding rhythms but Bmal1 deletion also affects amplitude and phase of translation, including TISU genes. Together this study emphasizes the complex interconnections between circadian and feeding rhythms at several steps ultimately determining rhythmic gene expression and translation.

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Multi-level remodelling of chromatin underlying activation of human T cells

Scientific Reports ◽

10.1038/s41598-020-80165-9 ◽

2021 ◽

Vol 11 (1) ◽

Author(s):

Naiara G. Bediaga ◽

Hannah D. Coughlan ◽

Timothy M. Johanson ◽

Alexandra L. Garnham ◽

Gaetano Naselli ◽

...

Keyword(s):

Gene Expression ◽

T Cells ◽

T Cell ◽

T Cell Activation ◽

Cell Activation ◽

Chromatin Accessibility ◽

Chromatin Architecture ◽

Chromatin Interactions ◽

Human T Cells ◽

Multi Level

AbstractRemodelling of chromatin architecture is known to regulate gene expression and has been well characterized in cell lineage development but less so in response to cell perturbation. Activation of T cells, which triggers extensive changes in transcriptional programs, serves as an instructive model to elucidate how changes in chromatin architecture orchestrate gene expression in response to cell perturbation. To characterize coordinate changes at different levels of chromatin architecture, we analyzed chromatin accessibility, chromosome conformation and gene expression in activated human T cells. T cell activation was characterized by widespread changes in chromatin accessibility and interactions that were shared between activated CD4+ and CD8+ T cells, and with the formation of active regulatory regions associated with transcription factors relevant to T cell biology. Chromatin interactions that increased and decreased were coupled, respectively, with up- and down-regulation of corresponding target genes. Furthermore, activation was associated with disruption of long-range chromatin interactions and with partitioning of topologically associating domains (TADs) and remodelling of their TAD boundaries. Newly formed/strengthened TAD boundaries were associated with higher nucleosome occupancy and lower accessibility, linking changes in lower and higher order chromatin architecture. T cell activation exemplifies coordinate multi-level remodelling of chromatin underlying gene transcription.

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Impact of 3D genome organization, guided by cohesin and CTCF looping, on sex-biased chromatin interactions and gene expression in mouse liver

10.21203/rs.2.23342/v2 ◽

2020 ◽

Author(s):

Bryan J Matthews ◽

David J Waxman

Keyword(s):

Gene Expression ◽

Sex Differences ◽

Binding Sites ◽

Genome Organization ◽

Mouse Liver ◽

Ctcf Binding ◽

Gene Promoters ◽

3D Genome ◽

Chromatin Interactions ◽

The Impact

Abstract Several thousand sex-differential distal enhancers have been identified in mouse liver; however, their links to sex-biased genes and the impact of any sex-differences in nuclear organization and chromatin interactions are unknown. To address these issues, we first characterized 1,847 mouse liver genomic regions showing significant sex differential occupancy by cohesin and CTCF, two key 3D nuclear organizing factors. These sex-differential binding sites were primarily distal to sex-biased genes but rarely generated sex-differential TAD (topologically associating domain) or intra-TAD loop anchors, and were sometimes found in TADs without sex-biased genes. A substantial subset of sex-biased cohesin-non-CTCF binding sites, but not sex-biased cohesin-and-CTCF binding sites, overlapped sex-biased enhancers. Cohesin depletion reduced the expression of male-biased genes with distal, but not proximal, sex-biased enhancers by >10-fold, implicating cohesin in long-range enhancer interactions regulating sex-biased genes. Using circularized chromosome conformation capture-based sequencing (4C-seq), we showed that sex differences in distal sex-biased enhancer - promoter interactions are common. Intra-TAD loops with sex-independent cohesin-and-CTCF anchors conferred sex specificity to chromatin interactions indirectly, by insulating sex-biased enhancer - promoter contacts and by bringing sex-biased genes into closer proximity to sex-biased enhancers. Furthermore, sex-differential chromatin interactions involving sex-biased gene promoters, enhancers, and lncRNAs were associated with sex-biased binding of cohesin and/or CTCF. These studies elucidate how 3D genome organization impacts sex-biased gene expression in a non-reproductive tissue through both direct and indirect effects of cohesin and CTCF looping on distal enhancer interactions with sex-differentially expressed genes.

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Impact of 3D genome organization, guided by cohesin and CTCF looping, on sex-biased chromatin interactions and gene expression in mouse liver

10.21203/rs.2.23342/v3 ◽

2020 ◽

Author(s):

Bryan J Matthews ◽

David J Waxman

Keyword(s):

Gene Expression ◽

Sex Differences ◽

Binding Sites ◽

Genome Organization ◽

Mouse Liver ◽

Ctcf Binding ◽

Gene Promoters ◽

3D Genome ◽

Chromatin Interactions ◽

The Impact

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Understanding 3D Genome Organization and Its Effect on Transcriptional Gene Regulation Under Environmental Stress in Plant: A Chromatin Perspective

Frontiers in Cell and Developmental Biology ◽

10.3389/fcell.2021.774719 ◽

2021 ◽

Vol 9 ◽

Author(s):

Suresh Kumar ◽

Simardeep Kaur ◽

Karishma Seem ◽

Santosh Kumar ◽

Trilochan Mohapatra

Keyword(s):

Gene Expression ◽

Environmental Stress ◽

Genome Organization ◽

Regulation Of Gene Expression ◽

Three Dimensional ◽

Regulatory Elements ◽

Chromosome Conformation ◽

3D Genome ◽

Chromatin Architecture ◽

Capture Techniques

The genome of a eukaryotic organism is comprised of a supra-molecular complex of chromatin fibers and intricately folded three-dimensional (3D) structures. Chromosomal interactions and topological changes in response to the developmental and/or environmental stimuli affect gene expression. Chromatin architecture plays important roles in DNA replication, gene expression, and genome integrity. Higher-order chromatin organizations like chromosome territories (CTs), A/B compartments, topologically associating domains (TADs), and chromatin loops vary among cells, tissues, and species depending on the developmental stage and/or environmental conditions (4D genomics). Every chromosome occupies a separate territory in the interphase nucleus and forms the top layer of hierarchical structure (CTs) in most of the eukaryotes. While the A and B compartments are associated with active (euchromatic) and inactive (heterochromatic) chromatin, respectively, having well-defined genomic/epigenomic features, TADs are the structural units of chromatin. Chromatin architecture like TADs as well as the local interactions between promoter and regulatory elements correlates with the chromatin activity, which alters during environmental stresses due to relocalization of the architectural proteins. Moreover, chromatin looping brings the gene and regulatory elements in close proximity for interactions. The intricate relationship between nucleotide sequence and chromatin architecture requires a more comprehensive understanding to unravel the genome organization and genetic plasticity. During the last decade, advances in chromatin conformation capture techniques for unravelling 3D genome organizations have improved our understanding of genome biology. However, the recent advances, such as Hi-C and ChIA-PET, have substantially increased the resolution, throughput as well our interest in analysing genome organizations. The present review provides an overview of the historical and contemporary perspectives of chromosome conformation capture technologies, their applications in functional genomics, and the constraints in predicting 3D genome organization. We also discuss the future perspectives of understanding high-order chromatin organizations in deciphering transcriptional regulation of gene expression under environmental stress (4D genomics). These might help design the climate-smart crop to meet the ever-growing demands of food, feed, and fodder.

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Impact of 3D genome organization, guided by cohesin and CTCF looping, on sex-biased chromatin interactions and gene expression in mouse liver

Epigenetics & Chromatin ◽

10.1186/s13072-020-00350-y ◽

2020 ◽

Vol 13 (1) ◽

Author(s):

Bryan J. Matthews ◽

David J. Waxman

Keyword(s):

Gene Expression ◽

Genome Organization ◽

Mouse Liver ◽

3D Genome ◽

Chromatin Interactions

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Intron-driven gene expression in the absence of a core promoter in Arabidopsis thaliana

10.1101/083261 ◽

2016 ◽

Author(s):

Jenna E Gallegos ◽

Alan B Rose

Keyword(s):

Gene Expression ◽

Rna Polymerase Ii ◽

Transcription Initiation ◽

Core Promoter ◽

Regulatory Elements ◽

Intron Position ◽

Mrna Accumulation ◽

Practical Applications ◽

Promoter Sequences ◽

The Core

AbstractIn diverse eukaryotes, certain introns increase mRNA accumulation through the poorly understood mechanism of intron-mediated enhancement (IME). A distinguishing feature of IME is that these introns have no effect from upstream or more than 1 Kb downstream of the transcription start site (TSS). To more precisely define the intron position requirements for IME in Arabidopsis, we tested the effect of the UBQ10 intron on gene expression from 6 different positions surrounding the TSS of a TRP1:GUS fusion. The intron strongly increased expression from all transcribed positions, but had no effect when 204 nt or more upstream of the 5’-most TSS. When the intron was located in the 5’ UTR, the TSS unexpectedly changed, resulting in longer transcripts. Remarkably, deleting 303 nt of the core promoter, including all known TSS’s and all but 18 nt of the 5’ UTR, had virtually no effect on the level of gene expression as long as a stimulating intron was included in the gene. When the core promoter was deleted, transcription initiated in normally untranscribed sequences the same distance upstream of the intron as when the promoter was intact. Together, these results suggest that certain introns play unexpectedly large roles in directing transcription initiation and represent a previously unrecognized type of downstream regulatory elements for genes transcribed by RNA polymerase II. This study also demonstrates considerable flexibility in the sequences surrounding the TSS, indicating that the TSS is not determined by promoter sequences alone. These findings are relevant in practical applications where introns are used to increase gene expression and contribute to our general understanding of gene structure and regulation in eukaryotes.

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