Dynamic Polycomb-CBC crosstalk orchestrates mRNA production at transcriptionally active loci in plants

Histone modifications and cotranscriptional processing play fundamental roles in regulating eukaryotic gene transcription. Active histone modifications and efficient cotranscriptional mRNA processing act in concert to promote transcription, whereas repressive histone marks are normally depleted from active genes. However, the localization of repressive histone marks at transcribing genes and the regulatory mechanism in mRNA transcription are largely unclear. Here, we show that in Arabidopsis thaliana, the chromodomain H3K27me3 reader LIKE HETEROCHROMATIN PROTEIN1 binds nascent precursor mRNA through its middle intrinsically disordered region at H3K27me3-coated chromatin loci, thereby attenuating transcription efficiency. This interaction is subsequently disrupted by mRNA cap-binding complex to complete transcription. We illustrate how this interplay fine-tunes WUSCHEL transcription in the shoot apical meristem region to maintain stem cell homeostasis. Our findings uncover a distinct mechanism implemented by Polycomb repression and elucidates an interdependent crosstalk linking repressive histone modification and cotranscriptional mRNA processing to transcription regulation.