TOP1α regulates FLOWERING LOCUS C expression by coupling histone modification and transcription machinery

The key steps of transcription are coupled with the opening of the DNA helical structure and establishment of active chromatin to facilitate the movement of the transcription machinery. Type I topoisomerases cleave one DNA strand and relax the supercoiled structure of transcribed templates. How topoisomerase-mediated DNA topological changes promote transcription and establish a permissive histone modification for transcription elongation is largely unknown. Here, we show that TOPOISOMERASE 1 alpha in plants regulates FLOWERING LOCUS C transcription by coupling histone modification and transcription machinery. We demonstrate that TOP1 alpha directly interacts with the methyltransferase SDG8 to establish high levels of H3K36 methylation downstream of FLC transcription start sites and recruits RNA polymerase II to facilitate transcription elongation. Our results provide a mechanistic framework for TOP1a control of the main steps of early transcription and demonstrate how topoisomerases couple RNA polymerase II and permissive histone modifications to initiate transcription elongation.