Mutually exclusive sense–antisense transcription at FLC facilitates environmentally induced gene repression

Rosa, Stefanie; Duncan, Susan; Dean, Caroline

doi:10.1038/ncomms13031

Cited by 129 publications

(133 citation statements)

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“…Thus, it has been hypothesized that the antisense transcript COOLAIR acts in cis. Indeed, recent singlemolecule RNA FISH showed that COOLAIR and FLC sense transcription is mutually exclusive and confirmed that COOLAIR acts in cis to silence FLC during cold (32). Comparison of the A. thaliana and Arabidopsis alpina FLC antisense promoter regions revealed DNA sequence conservation, and an analogous antisense transcript was also detected in the latter species (33).…”

Section: Significancementioning

confidence: 89%

“…Examples of cis-acting antisense mechanisms include Xist-mediated allele-specific X-chromosome inactivation in humans and PHO gene regulation in yeast (54,55). In addition, it has been suggested that in plants the antisense transcript COOLAIR acts via the process of its transcription or by formation of an RNA cloud, as seen in single-molecule FISH suppressing FLC transcription in cis (22,32).…”

Section: Dog1 Antisense Is a Suppressor Of Seed Dormancy In Arabidopsismentioning

confidence: 99%

See 1 more Smart Citation

Control of seed dormancy in Arabidopsis by a cis -acting noncoding antisense transcript

Fedak

Palusińska

Krzyczmonik

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

128

168

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Seed dormancy is one of the most crucial process transitions in a plant's life cycle. Its timing is tightly controlled by the expression level of the Delay of Germination 1 gene (DOG1). DOG1 is the major quantitative trait locus for seed dormancy in Arabidopsis and has been shown to control dormancy in many other plant species. This is reflected by the evolutionary conservation of the functional short alternatively polyadenylated form of the DOG1 mRNA. Notably, the 3′ region of DOG1, including the last exon that is not included in this transcript isoform, shows a high level of conservation at the DNA level, but the encoded polypeptide is poorly conserved. Here, we demonstrate that this region of DOG1 contains a promoter for the transcription of a noncoding antisense RNA, asDOG1, that is 5′ capped, polyadenylated, and relatively stable. This promoter is autonomous and asDOG1 has an expression profile that is different from known DOG1 transcripts. Using several approaches we show that asDOG1 strongly suppresses DOG1 expression during seed maturation in cis, but is unable to do so in trans. Therefore, the negative regulation of seed dormancy by asDOG1 in cis results in allele-specific suppression of DOG1 expression and promotes germination. Given the evolutionary conservation of the asDOG1 promoter, we propose that this cis-constrained noncoding RNA-mediated mechanism limiting the duration of seed dormancy functions across the Brassicaceae.seed dormancy | DOG1 gene | cis-acting ncRNA | antisense transcript P lants have evolved elaborate adaptation mechanisms to cope with unexpected and rapid changes in their natural environment (1). The division of the plant life cycle into consecutive developmental phases can be viewed as one such mechanism. This compartmentalization allows plants to focus their resources on particular tasks. The most pronounced developmental phases in plant development are seed dormancy, the juvenile phase, vegetative growth, flowering, and senescence (2). The transition between each successive phase has to be tightly controlled and aligned with the plant's internal metabolic state and external conditions.Seeds are characterized by their remarkable ability to withstand harsh environmental conditions (3). This is in part because of a seed dormancy mechanism that imposes a block on the ability of seeds to sense permissive conditions and initiate germination (4, 5). This mechanism allows seeds to temporarily bypass favorable conditions to germinate in an environment that will support the entire plant life cycle. Seed dormancy is under strong evolutionary selection because the improper timing of germination often results in immediate death (6). In addition, from an agronomical point of view, seed dormancy has been a subject of intensive selection, because on the one hand strong dormancy leads to uneven germination, but on the other hand weak dormancy may result in preharvest sprouting because of germination on the mother plant (7).An analysis of seed dormancy variability among Arabidopsis thaliana ac...

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Section: Significancementioning

confidence: 89%

Section: Dog1 Antisense Is a Suppressor Of Seed Dormancy In Arabidopsismentioning

confidence: 99%

Control of seed dormancy in Arabidopsis by a cis -acting noncoding antisense transcript

Fedak

Palusińska

Krzyczmonik

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

128

168

View full text Add to dashboard Cite

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“…Our research suggests that the cryptic lncRNA component in such cascades could be identified by transcript profiling in nuclear exosome mutants. The lncRNA-mediated effects of long-term cold exposure on plant gene expression have been well characterized for the FLC gene 2,40 . Our research demonstrates that lncRNAs also mediate the response to short-term and transient cold exposure by timing maximal gene expression.…”

Section: Discussionmentioning

confidence: 99%

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

Kindgren

Ard

Ivanov

2018

Preprint

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SummaryMost DNA in the genomes of higher organisms does not encode proteins, but is transcribed by RNA polymerase II (RNAPII) into long non-coding RNA (lncRNA). The biological significance of most lncRNA is largely unclear. Here, we identify a lncRNA (SVALKA) in a cold-sensitive region of the Arabidopsis genome. Mutations in SVALKA affect the timing of maximal CBF1 expression and freezing tolerance. RNAPII read-through transcription of SVALKA results in a cryptic lncRNA overlapping CBF1 on the antisense strand, termed asCBF1. asCBF1 transcription is anti-correlated with CBF1 expression. Our molecular dissection reveals that CBF1 is suppressed by RNAPII collision stemming from the SVALKA-asCBF1 lncRNA cascade. The SVK-asCBF1 cascade provides a mechanism to tightly control CBF1 expression and timing that could be exploited to maximize freezing tolerance with mitigated fitness costs. Inversion of the transcriptional direction of a lncRNA cascade relative to the genes in a co-regulated cluster provides an elegant inbuilt negative feedback for cluster expression. Our results provide a compelling example of local gene regulation by lncRNA transcription having a profound impact on the ability of plants to appropriately acclimate to suboptimal environmental conditions. not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was . http://dx.doi.org/10.1101/287946 doi: bioRxiv preprint first posted online Mar. 23, 2018; Main RNA Polymerase II (RNAPII) transcription in genomes results in the production of many long noncoding RNAs (lncRNAs) 1 . The functional significance of resulting lncRNA molecules is actively debated even though biological roles are identified for an increasing number of examples [2][3][4] . Expression of lncRNAs is remarkably specific to the environmental condition, tissue or cell type, arguing for roles of lncRNA in regulation [5][6][7] . In addition to functions carried out by lncRNA molecules, the process of transcribing non-coding DNA sequences can by itself be regulatory in many systems 8,9 . Non-coding DNA regions in genomes can therefore affect gene expression by different mechanisms that need to be resolved experimentally.Sessile organisms respond to changing environmental conditions with regulation of gene expression. Early events in the Arabidopsis cold response include rapid transcriptional upregulation of the intron-less C-repeat/dehydration-responsive element binding factors (CBFs) 10,11 . The CBFs are highly conserved transcription factors that promote cold tolerance in many plant species and are often arranged in a single cluster 12. CBF expression during cold exposure activates downstream COLD REGULATED (COR) genes that promote freezing tolerance by adjusting the physiological and biochemical properties of plant cell interiors [13][14][15] . Intriguingly, constitutive CBF expression increases cold-tolerance but is also associated with fitness penalties [16][17][18][19] . antisense CBF1 lncRNA (...

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“…To date we have used the tool, and its nascent precursors, on over fifteen internal projects at various stages of the publication pipeline (Berry et al, 2015; Duncan et al, 2016; Rosa, Duncan & Dean, 2016). As the package has matured, we have found substantial gains in our productivity.…”

Section: Resultsmentioning

confidence: 99%

jicbioimage: a tool for automated and reproducible bioimage analysis

Olsson

Hartley

2016

PeerJ

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There has been steady improvement in methods for capturing bioimages. However analysing these images still remains a challenge. The Python programming language provides a powerful and flexible environment for scientific computation. It has a wide range of supporting libraries for image processing but lacks native support for common bioimage formats, and requires specific code to be written to ensure that suitable audit trails are generated and analyses are reproducible. Here we describe the development of a Python tool that: (1) allows users to quickly view and explore microscopy data; (2) generate reproducible analyses, encoding a complete history of image transformations from raw data to final result; and (3) scale up analyses from initial exploration to high throughput processing pipelines, with a minimal amount of extra effort. The tool, jicbioimage, is open source and freely available online at .

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Mutually exclusive sense–antisense transcription at FLC facilitates environmentally induced gene repression

Cited by 129 publications

References 28 publications

Control of seed dormancy in Arabidopsis by a cis -acting noncoding antisense transcript

Control of seed dormancy in Arabidopsis by a cis -acting noncoding antisense transcript

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

jicbioimage: a tool for automated and reproducible bioimage analysis

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