The transcription factor Sfp1 imprints specific classes of mRNAs and links their synthesis and cytoplasmic decay

Abstract

AbstractTo properly function as an integrated system, both transcriptional and post-transcriptional machineries must communicate; the underlying mechanisms are poorly understood. Here we focus on ribosomal biosynthetic and ribosomal protein genes, transcription of which is regulated by a promoter-binding transcription factor, Sfp1. We show that Sfp1 also binds their gene bodies, affecting RNA polymerase II (Pol II) configuration, leading to enhanced backtracking and Rpb4 dissociation. Unexpectedly, we discovered that Sfp1 binds a group of those mRNAs encoded by Sfp1-bound genes. Remarkably, Sfp1 regulates deadenylation and decay of its bound mRNAs. The interaction of Sfp1 with its client mRNAs is controlled by their respective promoters and occurs concomitantly with its dissociation from chromatin. Collectively, our data suggest that for a subset of its targets, Sfp1 accompanies Pol II and controls its configuration during elongation, moves to the emerging transcripts co-transcriptionally and regulates their cytoplasmic stability. Thus, Sfp1 co-transcriptional binding imprints mRNA fate and serves as a paradigm for a cross-talk between synthesis and decay of specific mRNAs.