Chromatin-based mechanisms to coordinate convergent overlapping transcription

In eukaryotic genomes, transcription units of genes often overlap with other protein-coding and/or noncoding transcription units. In such intertwined genomes, coordinated transcription of nearby or overlapping genes would be important to ensure integrity of genome function; however, the mechanisms underlying this coordination are largely unknown. Here, we show in Arabidopsis thaliana that genes with convergent orientation of transcription are major sources of overlapping bidirectional transcripts and that these bidirectionally transcribed genes are regulated by a putative LSD1 family histone demethylase, FLD. Our genome-wide chromatin profiling revealed that FLD, as well as its candidate cofactors LD and SDG26, downregulated histone H3K4me1 in regions with convergent overlapping transcription. FLD localizes to actively transcribed genes where it colocalizes with elongating RNA polymerase II phosphorylated at Ser-2 or Ser-5 sites. Genome-wide transcription analyses suggest that FLD-mediated H3K4me1 removal negatively regulates bidirectional transcription by retaining the elongating transcription machinery. Furthermore, this effect of FLD on transcription dynamics is mediated by DNA topoisomerase I. Our study has revealed chromatin-based mechanisms to cope with overlapping bidirectional transcription, which may occur by modulating DNA topology. This global mechanism to cope with bidirectional transcription could be co-opted for specific epigenetic processes, such as cellular memory of responses to environment.