Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation

Kindgren, Peter; Ard, Ryan; Ivanov, Maxim; Marquardt, Sebastian

doi:10.1038/s41467-018-07010-6

Cited by 182 publications

(190 citation statements)

References 61 publications

(68 reference statements)

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“…To investigate the in vivo RNAPII transcription speed of Arabidopsis RNAPII carrying the NRPB2 Y732F mutation, we developed an assay to monitor nascent RNAPII elongation after rapid transcription induction. To avoid time‐consuming sample handling and processing issues associated with RNAPII chromatin immunoprecipitation from plants (RNAPII‐ChIP) , we analyzed nascent RNA attached to RNAPII to monitor RNAPII elongation . We identified three pathogen resistance‐related Toll/interleukin receptor (TIR)‐type NB‐LRR genes AT4G19520 , AT5G41740, and AT5G41750 that are rapidly induced by flagellin 22 treatment.…”

Section: Resultsmentioning

confidence: 99%

Organismal benefits of transcription speed control at gene boundaries

et al. 2020

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RNA polymerase II (RNAPII) transcription is crucial for gene expression. RNAPII density peaks at gene boundaries, associating these key regions for gene expression control with limited RNAPII movement. The connections between RNAPII transcription speed and gene regulation in multicellular organisms are poorly understood. Here, we directly modulate RNAPII transcription speed by point mutations in the second largest subunit of RNAPII in Arabidopsis thaliana. A RNAPII mutation predicted to decelerate transcription is inviable, while accelerating RNAPII transcription confers phenotypes resembling auto‐immunity. Nascent transcription profiling revealed that RNAPII complexes with accelerated transcription clear stalling sites at both gene ends, resulting in read‐through transcription. The accelerated transcription mutant NRPB2‐Y732F exhibits increased association with 5′ splice site (5′SS) intermediates and enhanced splicing efficiency. Our findings highlight potential advantages of RNAPII stalling through local reduction in transcription speed to optimize gene expression for the development of multicellular organisms.

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Section: Resultsmentioning

confidence: 99%

Organismal benefits of transcription speed control at gene boundaries

et al. 2020

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“…LncRNAs have been implicated in cold and freeze response mechanisms in both plant and animal systems. Colddependent differential expression and differential alternative splicing of lncRNAs have been shown to correlate with acclimation and freeze tolerance in Arabidopsis [66,67]. Moreover, differential expression of lncRNA transcripts and associated target genes involved in cold response and apoptosis in frozen and thawed giant panda (Ailuropoda melanoleuca) sperm exhibited co-expression regulatory patterns, suggesting a role for the interaction between lncRNAs and their target mRNAs in cryopreservation, and as an extension, freeze tolerance [68].…”

Section: Differential Expression Of Non-coding Rnasmentioning

confidence: 99%

Hepatic transcriptome of the freeze-tolerant Cope’s gray treefrog, Dryophytes chrysoscelis: responses to cold acclimation and freezing

et al. 2020

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Background: Cope's gray treefrog, Dryophytes chrysoscelis, withstands the physiological challenges of corporeal freezing, partly by accumulating cryoprotective compounds of hepatic origin, including glycerol, urea, and glucose. We hypothesized that expression of genes related to cryoprotectant mobilization and stress tolerance would be differentially regulated in response to cold. Using high-throughput RNA sequencing (RNA-Seq), a hepatic transcriptome was generated for D. chrysoscelis, and gene expression was compared among frogs that were warmacclimated, cold-acclimated, and frozen. Results: A total of 159,556 transcripts were generated; 39% showed homology with known transcripts, and 34% of all transcripts were annotated. Gene-level analyses identified 34,936 genes, 85% of which were annotated. Cold acclimation induced differential expression both of genes and non-coding transcripts; freezing induced few additional changes. Transcript-level analysis followed by gene-level aggregation revealed 3582 differentially expressed genes, whereas analysis at the gene level revealed 1324 differentially regulated genes. Approximately 3.6% of differentially expressed sequences were non-coding and of no identifiable homology. Expression of several genes associated with cryoprotectant accumulation was altered during cold acclimation. Of note, glycerol kinase expression decreased with cold exposure, possibly promoting accumulation of glycerol, whereas glucose export was transcriptionally promoted by upregulation of glucose-6-phosphatase and downregulation of genes of various glycolytic enzymes. Several genes related to heat shock protein response, DNA repair, and the ubiquitin proteasome pathway were upregulated in cold and frozen frogs, whereas genes involved in responses to oxidative stress and anoxia, both potential sources of cellular damage during freezing, were downregulated or unchanged.

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“…RNA with potential to trigger siRNA-mediated gene silencing, or by transcriptional interference via RNAPII collision [46]. The tex1 and hpr1 mutant are known to have multiple phenotypes, ranging from defects in vegetative and reproductive development [18,38], responses to both biotic and abiotic stress [36,37] and the expression of genes encoding acid phosphatases [16] or ethylene signaling pathway repressor [20].…”

Section: Plos Geneticsmentioning

confidence: 99%

The transcription and export complex THO/TREX contributes to transcription termination in plants

et al. 2020

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Transcription termination has important regulatory functions, impacting mRNA stability, localization and translation potential. Failure to appropriately terminate transcription can also lead to read-through transcription and the synthesis of antisense RNAs which can have profound impact on gene expression. The Transcription-Export (THO/TREX) protein complex plays an important role in coupling transcription with splicing and export of mRNA. However, little is known about the role of the THO/TREX complex in the control of transcription termination. In this work, we show that two proteins of the THO/TREX complex, namely TREX COMPONENT 1 (TEX1 or THO3) and HYPER RECOMBINATION1 (HPR1 or THO1) contribute to the correct transcription termination at several loci in Arabidopsis thaliana. We first demonstrate this by showing defective termination in tex1 and hpr1 mutants at the nopaline synthase (NOS) terminator present in a T-DNA inserted between exon 1 and 3 of the PHO1 locus in the pho1-7 mutant. Read-through transcription beyond the NOS terminator and splicing-out of the T-DNA resulted in the generation of a near full-length PHO1 mRNA (minus exon 2) in the tex1 pho1-7 and hpr1 pho1-7 double mutants, with enhanced production of a truncated PHO1 protein that retained phosphate export activity. Consequently, the strong reduction of shoot growth associated with the severe phosphate deficiency of the pho1-7 mutant was alleviated in the tex1 pho1-7 and hpr1 pho1-7 double mutants. Additionally, we show that RNA termination defects in tex1 and hpr1 mutants leads to 3'UTR extensions in several endogenous genes. These results demonstrate that THO/ TREX complex contributes to the regulation of transcription termination.

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Transcriptional read-through of the long non-coding RNA SVALKA governs plant cold acclimation

Cited by 182 publications

References 61 publications

Organismal benefits of transcription speed control at gene boundaries

Organismal benefits of transcription speed control at gene boundaries

Hepatic transcriptome of the freeze-tolerant Cope’s gray treefrog, Dryophytes chrysoscelis: responses to cold acclimation and freezing

The transcription and export complex THO/TREX contributes to transcription termination in plants

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