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Evolutionarily conserved DEK domain‐containing proteins have been implicated in multiple chromatin‐related processes, mRNA splicing and transcriptional regulation in eukaryotes.

Here, we show that two DEK proteins, DEK3 and DEK4, control the floral transition inArabidopsis. DEK3 and DEK4 directly associate with chromatin of related flowering repressors,FLOWERING LOCUS C(FLC), and its two homologs,MADS AFFECTING FLOWERING4(MAF4) andMAF5, to promote their expression.

The binding of DEK3 and DEK4 to a histone octamerin vivoaffects histone modifications atFLC,MAF4andMAF5loci. In addition, DEK3 and DEK4 interact with RNA polymerase II and promote the association of RNA polymerase II withFLC,MAF4andMAF5chromatin to promote their expression.

Our results show that DEK3 and DEK4 directly interact with chromatin to facilitate the transcription of key flowering repressors and thus prevent precocious flowering inArabidopsis.

 

Vernalization accelerates flowering after prolonged winter cold. Transcriptional and epigenetic changes are known to be involved in the regulation of the vernalization response. Despite intensive applications of next‐generation sequencing in diverse aspects of plant research, genome‐wide transcriptome and epigenome profiling during the vernalization response has not been conducted. In this work, to our knowledge, we present the first comprehensive analyses of transcriptomic and epigenomic dynamics during the vernalization process inArabidopsis thaliana. Six major clusters of genes exhibiting distinctive features were identified. Temporary changes in histone H3K4me3 levels were observed that likely coordinate photosynthesis and prevent oxidative damage during cold exposure. In addition, vernalization induced a stable accumulation of H3K27me3 over genes encoding many development‐related transcription factors, which resulted in either inhibition of transcription or a bivalent status of the genes. Lastly,FLC‐like andVIN3‐like genes were identified that appear to be novel components of the vernalization pathway.

 

Chromatin structure is critical for gene expression and many other cellular processes. In Arabidopsis thaliana , the floral repressor FLC adopts a self-loop chromatin structure via bridging of its flanking regions. This local gene loop is necessary for active FLC expression. However, the molecular mechanism underlying the formation of this class of gene loops is unknown. Here, we report the characterization of a group of linker histone-like proteins, named the GH1-HMGA family in Arabidopsis , which act as chromatin architecture modulators. We demonstrate that these family members redundantly promote the floral transition through the repression of FLC . A genome-wide study revealed that this family preferentially binds to the 5′ and 3′ ends of gene bodies. The loss of this binding increases FLC expression by stabilizing the FLC 5′ to 3′ gene looping. Our study provides mechanistic insights into how a family of evolutionarily conserved proteins regulates the formation of local gene loops. 

The long noncoding RNA COLDAIR is necessary for the repression of a floral repressor FLOWERING LOCUS C (FLC) during vernalization in Arabidopsis thaliana. The repression of FLC is mediated by increased enrichment of Polycomb Repressive Complex 2 (PRC2) and subsequent trimethylation of Histone H3 Lysine 27 (H3K27me3) at FLC chromatin. In this study we found that the association of COLDAIR with chromatin occurs only at the FLC locus and that the central region of the COLDAIR transcript is critical for this interaction. A modular motif in COLDAIR is responsible for the association with PRC2 in vitro, and the mutations within the motif that reduced the association of COLDAIR with PRC2 resulted in vernalization insensitivity. The vernalization insensitivity caused by mutant COLDAIR was rescued by the ectopic expression of the wild-type COLDAIR. Our study reveals the molecular framework in which COLDAIR lncRNA mediates the PRC2-mediated repression of FLC during vernalization.