Vernalization-Triggered Intragenic Chromatin Loop Formation by Long Noncoding RNAs

Kim, Dong Hwan; Sung, Sibum

doi:10.1016/j.devcel.2016.12.021

Cited by 264 publications

(254 citation statements)

References 69 publications

(104 reference statements)

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“…The antisense lncRNA COOLAIR is induced after 2 weeks of cold, and initiates chromatin repression of the FLC gene 2,20 . Full FLC silencing is aided by polycomb repressive complex recruitment by the intronderived lncRNA COLDAIR and reinforced by the promoter derived lncRNA COLDWRAP 21 . This cold-triggered cascade of lncRNA establishes long-lasting and stable repression of the FLC gene and serves as a paradigm for gene repression by lncRNA 22 .…”

Section: Mainmentioning

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 not peer-reviewed) is the author/funder.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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Section: Mainmentioning

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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“…Antisense COOLAIR is a highly structured molecule (Hawkes et al ., ) that coats and downregulates the FLC locus upon cold exposure (Rosa et al ., ). Sense lncRNA COLDWRAP forms a repressive intragenic chromatin loop, whereas COLDAIR facilitates recruitment of Polycomb Repressive Complex 2 (PRC2) to FLC (Kim & Sung, ; Kim et al ., ). Another player is the sequence‐specific transcriptional repressor VIVIPAROUS1/ABI3‐LIKE1 (VAL1), which binds specifically to the PRC2 entry site at FLC , most likely to bring to the locus the repressive activity of this complex (Questa et al ., ).…”

Section: Convergence At Transcriptional Hubsmentioning

confidence: 99%

Light and temperature cues: multitasking receptors and transcriptional integrators

Casal

Qüesta

2017

New Phytologist

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Contents Summary1029I.Introduction1029II.Convergence at the receptor1030III.Convergence at transcriptional hubs1031IV.Convergence involving clock components1033V.Conclusions1033Acknowledgements1033References1033 Summary The combined information provided by light and temperature cues helps to optimise plant body architecture and physiology. Plants possess elaborate systems to sense and respond to these stimuli. Simultaneous perception of light and temperature by dual receptors such as phytochrome B and phototropin leads to immediate signalling convergence. Conversely, cue asynchronies initiate separate pathways and the information of the earliest cue is stored, awaiting the arrival of the later cue to control transcription. Storage mechanisms can involve changes in the activity of selected clock components or epigenetic modifications, depending on the time delay between cues (hours, days or several months). We propose a conceptual framework in which the mechanisms of integration relate to the timing of cue sensing.

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“…Several plant lncRNAs have been shown to regulate important biological processes: COLDAIR and COOLAIR specify flowering time by regulating the FLC locus (Liu et al ., ; Heo & Sung, ; Sun et al ., ), LONG DAY‐SPECIFIC MALE‐FERTILITY‐ASSOCIATED RNA ( LDMAR ) controls rice fertility (Ding et al ., ), HIDDEN TREASURE 1 ( HID1 ) is involved in photomorphogenesis by regulating PHYTOCHROME‐INTERACTING FACTOR 3 ( PIF3 ) (Wang et al ., ), eTM‐type lncRNA IPS1 acts as a miR399 target mimic in phosphate homeostasis (Franco‐Zorrilla et al ., ), ASCO lncRNA mediates alternative splicing by recruiting related regulators (Bardou et al ., ) and AUXIN REGULATED PROMOTER LOOP ( APOLO ) regulates polar auxin transport by controlling chromatin loop dynamics (Ariel et al ., ). An additional lncRNA, COLDWRAP has been recently identified from the repressed FLC promoter during vernalization (Kim & Sung, ). This lncRNA is involved in the formation of a repressive chromatin loop critical for maintaining the polycomb‐medicated silencing of FLC .…”

Section: Introductionmentioning

confidence: 99%

A noncoding RNA transcribed from the AGAMOUS (AG) second intron binds to CURLY LEAF and represses AG expression in leaves

Deng

et al. 2018

New Phytologist

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Dispersed H3K27 trimethylation (H3K27me3) of the AGAMOUS (AG) genomic locus is mediated by CURLY LEAF (CLF), a component of the Polycomb Repressive Complex (PRC) 2. Previous reports have shown that the AG second intron, which confers AG tissue-specific expression, harbors sequences targeted by several positive and negative regulators. Using RACE reverse transcription polymerase chain reaction, we found that the AG intron 2 encodes several noncoding RNAs. RNAi experiment showed that incRNA4 is needed for CLF repressive activity. AG-incRNA4RNAi lines showed increased leaf AG mRNA levels associated with a decrease of H3K27me3 levels; these plants displayed AG overexpression phenotypes. Genetic and biochemical analyses demonstrated that the AG-incRNA4 can associate with CLF to repress AG expression in leaf tissues through H3K27me3-mediated repression and to autoregulate its own expression level. The mechanism of AG-incRNA4-mediated repression may be relevant to investigations on tissue-specific expression of Arabidopsis MADS-box genes.

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Vernalization-Triggered Intragenic Chromatin Loop Formation by Long Noncoding RNAs

Cited by 264 publications

References 69 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

Light and temperature cues: multitasking receptors and transcriptional integrators

A noncoding RNA transcribed from the AGAMOUS (AG) second intron binds to CURLY LEAF and represses AG expression in leaves

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