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Intronic long noncoding RNAs activate host gene expression by affecting histone modification in Arabidopsis (smallRNA-seq)

ABSTRACT: Intronic RNAs are spliced from precursor-messenger RNAs and are usually subjected to degradation in eukaryotes. COLDAIR, a previously reported intronic long noncoding RNA (lncRNA), is produced from the first intron of a MADS-box gene, Flowering Locus C (FLC), which encodes a repressor of flowering time. Here we show that overexpression of a foreign COLDAIR sequence causes enhanced expression of FLC in trans, resulting in a late-flowering phenotype. In COLDAIR-overexpression lines, enhanced expression of FLC is correlated with up-regulation of the active histone mark H3K4me3 and down-regulation of the repressive histone mark H3K27me3. We demonstrate that overexpression of COLDAIR makes the corresponding FLC intronic region accessible to the histone H3K4 methyltransferase ATX1 but exclusive to the histone H3K27 methyltransferase CLF. Furthermore, we demonstrate that overexpression of intronic lncRNAs from many other MADS-box genes also activate the expression of their host genes in trans, suggesting that intronic lncRNAs act as enhancer RNAs in many MADS-box genes. Considering that MADS-box genes are highly conserved in multicellular eukaryotes, we suggest that involvement of intronic lncRNAs from MADS-box genes in gene activation may represent an evolutionarily conserved mechanism.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE140138 | GEO | 2019/11/09

REPOSITORIES: GEO

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Project description:The transition to flowering in plants is controlled by a regulatory network that responds to both developmental and environmental signals. The MADS-box genes FLOWERING LOCUS C (FLC) and SHORT VEGETATIVE PHASE (SVP) are major flowering repressors that enhance responses to environmental cues such as winter temperatures, high ambient temperatures and photoperiod. FLC and SVP physically interact in vivo and mutation of each gene causes early flowering while the double mutant is more extreme. The molecular mechanisms underlying these genetic interactions are mostly unknown. We addressed the regulatory input of these two key transcription factors (TFs) both individually and as a complex at the genome-wide level through ChIP-seq and microarray expression analysis in single and double mutants. Analysis of each TF demonstrated that the complex acts predominantly via functional redundancy in the repression of flowering. SVP and FLC bind to the same regions of the flowering genes SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) and FLOWERING LOCUS T (FT) but do not require the presence of the other to bind. However, genome-wide identification of SVP and FLC occupancy events revealed that their binding scenarios are quantitatively and qualitatively affected by the presence of the cognate partner. A subgroup of genes whose regulation by these TFs depends exclusively on combinatorial binding of both proteins was identified, demonstrating a qualitatively essential role of the SVP-FLC complex. Some of these genes are involved in the control of flowering through direct and indirect regulation of Gibberellin-related processes. Cis-regulatory elements enriched only at such complex-bound sites were identified. Thus the regulatory output mediated by SVP and FLC reveals substantial flexibility, leading to dependent and independent DNA binding that enables additive, cooperative and repressive modes of co-regulation. In total 48 samples; 24 leaf samples corresponding to two different growing conditions, 24 apex samples corresponding to two different growing conditions.

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Intronic long noncoding RNAs activate host gene expression by affecting histone modification in Arabidopsis (smallRNA-seq)

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