Cytosolic acetyl-CoA promotes histone acetylation predominantly at H3K27 in Arabidopsis

Abstract

Acetyl-coenzyme A (acetyl-CoA) is a central metabolite and the acetyl source for protein acetylation, particularly histone acetylation that promotes gene expression. However, the effect of acetyl-CoA levels on histone acetylation status in plants remains unknown. Here, we show that malfunctioned cytosolic acetyl-CoA carboxylase1 (ACC1) in Arabidopsis leads to elevated levels of acetyl-CoA and promotes histone hyperacetylation predominantly at lysine 27 of histone H3 (H3K27). The increase of H3K27 acetylation (H3K27ac) is dependent on adenosine triphosphate (ATP)-citrate lyase which cleaves citrate to acetyl-CoA in the cytoplasm, and requires histone acetyltransferase GCN5. A comprehensive analysis of the transcriptome and metabolome in combination with the genome-wide H3K27ac profiles of acc1 mutants demonstrate the dynamic changes in H3K27ac, gene transcripts and metabolites occurring in the cell by the increased levels of acetyl-CoA. This study suggests that H3K27ac is an important link between cytosolic acetyl-CoA level and gene expression in response to the dynamic metabolic environments in plants.

Genome‐wide occupancy of histone H3K27 methyltransferases CURLY LEAF and SWINGER in Arabidopsis seedlings

“…ChIP experiments were carried out as described (Chen et al., ; Gendrel et al., ; Li et al., ) with minor modifications. For the ChIP with the transgenic plants clf‐29 pCLF::CLF‐GFP and swn‐4 pSWN::SWN‐GFP , another transgenic line that carries GFP only in WT genetic background ( p35S::GFP ) was used as the negative control.…”

“…The HiSeq 2500 platform was used for high‐throughput sequencing of the libraries. Sequence data were analyzed essentially as previously described (Chen et al., ; Li et al., , ). Briefly, after sequencing, the raw sequence reads were cleaned by removing bases with low quality score and cutting sequencing adapter followed by filtering out short reads.…”

“…The HiSeq 2500 platform was used for high-throughput sequencing of the libraries. Sequence data were analyzed essentially as previously described (Chen et al, 2017;Li et al, 2015.…”

Characterization of Arabidopsis thaliana promoter bidirectionality and antisense RNAs by depletion of nuclear RNA decay enzymes

“…The similarity of transcription initiation patterns between different RNA classes has spurred the hypothesis that RNA polymerase II is subject to the same rules regardless of the RNA that is produced, so that bidirectionally transcribed NDRs constitute a generic transcription initiation block, and the fate and function of RNAs produced are determined after transcription initiation (Chen et al, 2017;Andersson et al, 2015b) , also reviewed in .…”

“…To further characterize these bidirectionally transcribed loci, we assessed their chromatin state using published data: the majority of bidirectional CAGE sites overlapped with a DHS ( Figure 5E ) and were centered on accessible DNA, as measured by DNase and MNase-seq ( Figure 5F ). Histones adjacent to the NDRs were enriched for H3K27ac (Chen et al, 2017) and to a lesser degree, H3K4me1 and H3K4me3 (Wang et al, 2015;van Dijk et al, 2010) ( Figure 5G ).…”