Abstract
Progression of RNA polymerase II (RNAPII) transcription relies on the appropriately positioned activities of elongation factors. The resulting profile of factors and chromatin signatures along transcription units provides a “positional information system” for transcribing RNAPII. Here, we investigate a chromatin-based mechanism that suppresses intragenic initiation of RNAPII transcription. We demonstrate that RNAPII transcription across gene promoters represses their function in plants. This repression is characterized by reduced promoter-specific molecular signatures and increased molecular signatures associated with RNAPII elongation. The conserved FACT histone chaperone complex is required for this repression mechanism. Genome-wide Transcription Start Site (TSS) mapping reveals thousands of discrete intragenic TSS positions in fact mutants, including downstream promoters that initiate alternative transcript isoforms. We find that histone H3 lysine 4 mono-methylation (H3K4me1), an Arabidopsis RNAPII elongation signature, is enriched at FACT-repressed intragenic TSSs. Our analyses suggest that FACT is required to repress intragenic TSSs at positions that are in part characterized by elevated H3K4me1 levels. In sum, conserved and plant-specific chromatin features correlate with the co-transcriptional repression of intragenic TSSs. Our insights into TSS repression by RNAPII transcription promise to inform the regulation of alternative transcript isoforms and the characterization of gene regulation through the act of pervasive transcription across eukaryotic genomes.
Highlights
Plasticity at the beginning and end of transcription units multiplies the RNA species that can be generated from genomes
The position where transcription starts can be dynamically regulated to expand the diversity of RNA isoforms produced from a single gene
RT-qPCR analysis shows about 20-times higher RFD1 expression in rfd1-1 compared to wild type (Fig 1H), northern blotting reveals an abundant T-DNA-RFD1 compound transcript with increased transcript size in rfd1-1 initiating from the upstream T-DNA insertion (Fig 1I, S1D Fig) [53]
Summary
Plasticity at the beginning and end of transcription units multiplies the RNA species that can be generated from genomes. Metagene analyses of stage-specific transcription factors and chromatin signatures in diverse organisms strikingly visualize many common changes associated with RNAPII progression from the beginning to the end of active transcription units [12,13,14,15,16,17]. Histone 3 lysine 4 methylation (H3K4me) states decrease from tri- (H3K4me3) to mono-methylation (H3K4me1) from the beginning to the end of yeast genes [18]. Such signatures provide a “positional information system” (POINS) for RNAPII to coordinate molecular events required for each stage of transcription [8]
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