Repression of Cell Differentiation by a cis-Acting lincRNA in Fission Yeast

Fauquenoy, Sylvain; Migeot, Valérie; Finet, Olivier; Yague-Sanz, Carlo; Khorosjutina, Olga; Ekwall, Karl; Hermand, Damien

doi:10.1016/j.cub.2017.12.048

Cited by 18 publications

(29 citation statements)

References 51 publications

(68 reference statements)

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“…asCBF1 is likely representative of additional lncRNAs with regulatory roles that are challenging to study owing to their cryptic and environmental specific expression characteristics. Our findings of multiple lncRNAs acting together is in line with recent findings suggesting a coordinated effect of multiple lncRNAs to regulate meiosis in yeasts 46 , 47 . The combinations of multiple lncRNAs amplify the interfaces with regulatory potential and may increase precision of target regulation.…”

Section: Discussionsupporting

confidence: 92%

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

et al. 2018

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Most DNA in the genomes of higher organisms does not encode proteins, yet much is transcribed by RNA polymerase II (RNAPII) into long non-coding RNAs (lncRNAs). The biological significance of most lncRNAs is largely unclear. Here, we identify a lncRNA (SVALKA) in a cold-sensitive region of the Arabidopsis genome. Mutations in SVALKA affect CBF1 expression and freezing tolerance. RNAPII read-through transcription of SVALKA results in a cryptic lncRNA overlapping CBF1 on the antisense strand, termed asCBF1. Our molecular dissection reveals that CBF1 is suppressed by RNAPII collision stemming from the SVALKA-asCBF1 lncRNA cascade. The SVALKA-asCBF1 cascade provides a mechanism to tightly control CBF1 expression and timing that could be exploited to maximize freezing tolerance with mitigated fitness costs. 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 challenging environmental conditions.

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Section: Discussionsupporting

confidence: 92%

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

et al. 2018

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“…Our findings of multiple lncRNA acting together is line with recent findings suggesting a coordinated effect of multiple lncRNA to regulate meiosis in yeasts 41,42 . The combinations of not peer-reviewed) is the author/funder.…”

Section: Discussionsupporting

confidence: 80%

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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“…Another class of lncRNAs consists of antisense transcripts, that are produced from the DNA strand antisense to genes [ 14 ]. Several examples of regulatory antisense (as)lncRNAs acting on sense gene expression in cis or in trans have been described in the budding yeast Saccharomyces cerevisiae [ 15 , 16 , 17 , 18 , 19 , 20 , 21 ], in the fission yeast Schizosaccharomyces pombe [ 22 , 23 , 24 ], in plant [ 25 ] and in mammalian cells [ 26 , 27 ].…”

Section: Introductionmentioning

confidence: 99%

Bases of antisense lncRNA-associated regulation of gene expression in fission yeast

et al. 2018

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Antisense (as)lncRNAs can regulate gene expression but the underlying mechanisms and the different cofactors involved remain unclear. Using Native Elongating Transcript sequencing, here we show that stabilization of antisense Exo2-sensitivite lncRNAs (XUTs) results in the attenuation, at the nascent transcription level, of a subset of highly expressed genes displaying prominent promoter-proximal nucleosome depletion and histone acetylation. Mechanistic investigations on the catalase gene ctt1 revealed that its induction following oxidative stress is impaired in Exo2-deficient cells, correlating with the accumulation of an asXUT. Interestingly, expression of this asXUT was also activated in wild-type cells upon oxidative stress, concomitant to ctt1 induction, indicating a potential attenuation feedback. This attenuation correlates with asXUT abundance, it is transcriptional, characterized by low RNAPII-ser5 phosphorylation, and it requires an histone deacetylase activity and the conserved Set2 histone methyltransferase. Finally, we identified Dicer as another RNA processing factor acting on ctt1 induction, but independently of Exo2. We propose that asXUTs could modulate the expression of their paired-sense genes when it exceeds a critical threshold, using a conserved mechanism independent of RNAi.

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Repression of Cell Differentiation by a cis-Acting lincRNA in Fission Yeast

Cited by 18 publications

References 51 publications

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

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

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

Bases of antisense lncRNA-associated regulation of gene expression in fission yeast

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