Antisense COOLAIR mediates the coordinated switching of chromatin states at FLC during vernalization

Abstract

Long noncoding RNAs (lncRNAs) have been proposed to play important roles in gene regulation. However, their importance in epigenetic silencing and how specificity is determined remain controversial. We have investigated the cold-induced epigenetic switching mechanism involved in the silencing of Arabidopsis thaliana FLOWERING LOCUS C (FLC), which occurs during vernalization. Antisense transcripts, collectively named COOLAIR, are induced by prolonged cold before the major accumulation of histone 3 lysine 27 trimethylation (H3K27me3), characteristic of Polycomb silencing. We have found that COOLAIR is physically associated with the FLC locus and accelerates transcriptional shutdown of FLC during cold exposure. Removal of COOLAIR disrupted the synchronized replacement of H3K36 methylation with H3K27me3 at the intragenic FLC nucleation site during the cold. Consistently, genetic analysis showed COOLAIR and Polycomb complexes work independently in the cold-dependent silencing of FLC. Our data reveal a role for lncRNA in the coordinated switching of chromatin states that occurs during epigenetic regulation.flowering | long noncoding RNA | histone modifications | Polycomb | Arabidopsis

The Binding Specificity of the PHD-Finger Domain of VIN3 Moderates Vernalization Response

“…Natural variation studies identified multiple putative cis-elements within FLC locus that are necessary to mediate proper vernalization response (Li et al, 2014;Coustham et al, 2012). In addition, several noncoding RNAs have been reported to play roles in vernalization-mediated FLC repression (Heo and Sung, 2011;Csorba et al, 2014). Therefore, the vernalization response utilizes multiple regulatory modes to ensure that vernalization occurs in response to only prolonged cold of winter and the binding preference of VIN3-PHD finger also plays an important role in mediating proper vernalization response through monitoring the status of FLC chromatin.…”

Phylogenomic Synteny Network Analysis of MADS-Box Transcription Factor Genes Reveals Lineage-Specific Transpositions, Ancient Tandem Duplications, and Deep Positional Conservation

“…The vernalization process (prolonged cold exposure) is essential for many plants to initiate flowering. In Arabidopsis and other crucifers, this process is mediated by coldinduced epigenetic repression of FLC genes, namely, histone methylation (Bastow et al, 2004), chromatin structure modification with chromatin remodeling protein complexes (Kim and Sung, 2013), and the expression of long noncoding RNAs (Csorba et al, 2014). Genes flanking FLC are epigenetically coordinately regulated (Finnegan et al, 2004).…”

Physical coupling of activation and derepression activities to maintain an active transcriptional state at FLC

“…Both of these involve accumulation of high levels of H3K27me3 at FLC (20)(21)(22). A series of FLC antisense transcripts (COOLAIR) contribute to these repression pathways (18,(23)(24)(25)(26). Our previous work revealed that H3K36me3 is associated with an actively transcribed FLC ON state, opposing an H3K27me3 OFF state, where a high level of H3K27me3 across FLC maintains long-term silencing (18,23).…”

“…Both of these involve accumulation of high levels of H3K27me3 at FLC (20-22). A series of FLC antisense transcripts (COOLAIR) contribute to these repression pathways (18,(23)(24)(25)(26) Opposing H3K36me3 and H3K27me3 states are particularly interesting as previous theoretical analysis had predicted the existence of such opposing, mutually exclusive histone modification states (23,28). Such a system would be maintained by nonlinear positive feedback mechanisms that could give robust bistability, resistant to noise and DNA replication.…”