Transcript isoform sequencing reveals widespread promoter-proximal transcriptional termination in Arabidopsis

Thomas, Quentin; Ard, Ryan; Liu, Jinghan; Li, Bingnan; Wang, Jingwen; Marquardt, Sebastian

doi:10.1038/s41467-020-16390-7

Cited by 54 publications

(49 citation statements)

References 74 publications

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“…Interestingly, further analysis indicated that these SUMO binding sites were predominantly located around TSSs, including promoter-proximal regions and potential 5′ UTR regions ( Figure 1 C, Supplemental Figure 3 A). Because previous work indicated that these regions are critical for TF binding and transcription regulation ( Ohler and Wassarman, 2010 ; Shao and Zeitlinger, 2017 ; Thomas et al., 2020 ), our results suggest that SUMOylation may play a role in the modulation of gene transcription. By contrast, SUMO signals were weak in intergenic, transposon, and heterochromatin regions ( Supplemental Figure 4 ).…”

Section: Resultsmentioning

confidence: 57%

“…Our ChIP-seq data indicated that SUMO-associated chromatin peaks are predominantly located on promoter-TSS gene regions, which harbor active epigenetic markers ( Figure 1 D and 1F) ( He et al., 2011 ), suggesting that SUMOylation plays a role in transcriptional activation. Interestingly, these SUMO-enriched sites are preferentially localized around the TSS ( Figure 1 C), similar to the distribution of TFs ( Ohler and Wassarman, 2010 ; Shao and Zeitlinger, 2017 ; Thomas et al., 2020 ), such as HSFA1a ( Supplemental Figure 12 A). Consistently, predicted motifs in the HS SUMO peaks are also highly enriched in these regions ( Supplemental Figure 12 B).…”

Section: Discussionmentioning

confidence: 58%

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Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses

Han

Chen

Xia

et al. 2021

Plant Communications

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The post-translational protein modification known as SUMOylation has conserved roles in the heat stress responses of various species. The functional connection between the global regulation of gene expression and chromatin-associated SUMOylation in plant cells is unknown. Here, we uncovered a genome-wide relationship between chromatin-associated SUMOylation and transcriptional switches in Arabidopsis thaliana grown at room temperature, exposed to heat stress, and exposed to heat stress followed by recovery. The small ubiquitin-like modifier (SUMO)-associated chromatin sites, characterized by whole-genome ChIP-seq, were generally associated with active chromatin markers. In response to heat stress, chromatin-associated SUMO signals increased at promoter-transcriptional start site regions and decreased in gene bodies. RNA-seq analysis supported the role of chromatin-associated SUMOylation in transcriptional activation during rapid responses to high temperature. Changes in SUMO signals on chromatin were associated with the upregulation of heat-responsive genes and the downregulation of growth-related genes. Disruption of the SUMO ligase gene SIZ1 abolished SUMO signals on chromatin and attenuated rapid transcriptional responses to heat stress. The SUMO signal peaks were enriched in DNA elements recognized by distinct groups of transcription factors under different temperature conditions. These observations provide evidence that chromatin-associated SUMOylation regulates the transcriptional switch between development and heat stress response in plant cells.

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Section: Resultsmentioning

confidence: 57%

Section: Discussionmentioning

confidence: 58%

Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses

Han

Chen

Xia

et al. 2021

Plant Communications

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“…2E). Transcription of Arabidopsis genes frequently produces short promoter-proximal RNAs (sppRNA) which are sensitive to the HEN2 exonuclease and terminate about 100 nt downstream from the TSS [31]. We found that 5’ borders of genes called by TranscriptomeReconstructoR are in a better agreement with the sppRNA termination sites than 5’ borders of their annotated mates in both TAIR10 and Araport11 (Fig.…”

Section: Resultsmentioning

confidence: 96%

“…A representative example of such gene on Fig. S4 (see Additional File 2) demonstrates that its split nature can be further supported by independent TIF-seq dataset which detects both ends of mature RNA transcripts [31].…”

Section: Resultsmentioning

confidence: 99%

TrancriptomeReconstructoR: data-driven annotation of complex transcriptomes

Ivanov

Sandelin

Marquardt

2020

Preprint

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BackgroundThe quality of gene annotation determines the interpretation of results obtained in transcriptomic studies. The growing number of genome sequence information calls for experimental and computational pipelines for de novo transcriptome annotation. Ideally, gene and transcript models should be called from a limited set of key experimental data.ResultsWe developed TranscriptomeReconstructoR, an R package which implements a pipeline for automated transcriptome annotation. It relies on integrating features from independent and complementary datasets: i) full-length RNA-seq for detection of splicing patterns and ii) high-throughput 5’ and 3’ tag sequencing data for accurate definition of gene borders. The pipeline can also take a nascent RNA-seq dataset to supplement the called gene model with transient transcripts.We reconstructed de novo the transcriptional landscape of wild type Arabidopsis thaliana seedlings as a proof-of-principle. A comparison to the existing transcriptome annotations revealed that our gene model is more accurate and comprehensive than the two most commonly used community gene models, TAIR10 and Araport11. In particular, we identify thousands of transient transcripts missing from the existing annotations. Our new annotation promises to improve the quality of A.thaliana genome research.ConclusionsOur proof-of-concept data suggest a cost-efficient strategy for rapid and accurate annotation of complex eukaryotic transcriptomes. We combine the choice of library preparation methods and sequencing platforms with the dedicated computational pipeline implemented in the TranscriptomeReconstructoR package. The pipeline only requires prior knowledge on the reference genomic DNA sequence, but not the transcriptome. The package seamlessly integrates with Bioconductor packages for downstream analysis.

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“…On the other hand, evidence of transcriptional stalling via RNAPII backtracking triggering nucleolytic degradation of the nascent RNA indicates that TTSa-RNAs may be implied in the termination of mRNA transcription ( Valen et al, 2011 ). For instance, a recent study in A. thaliana indicated that promoter-proximal RNAPII stalling can regulate plant gene transcription ( Thomas et al, 2020 ). Thus, it is reasonable to infer that mammalian TTSa-RNAs might participate in the regulation of gene transcription through the modulation of transcriptional termination ( Figure 3 ).…”

Section: Functions Of Tanrsmentioning

confidence: 99%

Terminus-Associated Non-coding RNAs: Trash or Treasure?

Xie

Leng

2020

Front. Genet.

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3 untranslated regions (3 UTRs) of protein-coding genes are well known for their important roles in determining the fate of mRNAs in diverse processes, including trafficking, stabilization, translation, and RNA-protein interactions. However, non-coding RNAs (ncRNAs) scattered around 3 termini of the protein-coding genes, here referred to as terminus-associated non-coding RNAs (TANRs), have not attracted wide attention in RNA research. Indeed, whether TANRs are transcriptional noise, degraded mRNA products, alternative 3 UTRs, or functional molecules has remained unclear for a long time. As a new category of ncRNAs, TANRs are widespread, abundant, and conserved in diverse eukaryotes. The biogenesis of TANRs mainly follows the same promoter model, the RNA-dependent RNA polymerase activity-dependent model, or the independent promoter model. Functional studies of TANRs suggested that they are significantly involved in the versatile regulation of gene expression. For instance, at the transcriptional level, they can lead to transcriptional interference, induce the formation of gene loops, and participate in transcriptional termination. Furthermore, at the posttranscriptional level, they can act as microRNA sponges, and guide cleavage or modification of target RNAs. Here, we review current knowledge of the potential role of TANRs in the modulation of gene expression. In this review, we comprehensively summarize the current state of knowledge about TANRs, and discuss TANR nomenclature, relation to ncRNAs, cross-talk biogenesis pathways and potential functions. We further outline directions of future studies of TANRs, to promote investigations of this emerging and enigmatic category of RNA.

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Transcript isoform sequencing reveals widespread promoter-proximal transcriptional termination in Arabidopsis

Cited by 54 publications

References 74 publications

Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses

Chromatin-associated SUMOylation controls the transcriptional switch between plant development and heat stress responses

TrancriptomeReconstructoR: data-driven annotation of complex transcriptomes

Terminus-Associated Non-coding RNAs: Trash or Treasure?

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