Abstract
Termination of RNA polymerase II (RNAPII) transcription is a fundamental step of gene expression that is critical for determining the borders between genes. In budding yeast, termination at protein-coding genes is initiated by the cleavage/polyadenylation machinery, whereas termination of most noncoding RNA (ncRNA) genes occurs via the Nrd1–Nab3–Sen1 (NNS) pathway. Here, we find that NNS-like transcription termination is not conserved in fission yeast. Rather, genome-wide analyses show global recruitment of mRNA 3′ end processing factors at the end of ncRNA genes, including snoRNAs and snRNAs, and that this recruitment coincides with high levels of Ser2 and Tyr1 phosphorylation on the RNAPII C-terminal domain. We also find that termination of mRNA and ncRNA transcription requires the conserved Ysh1/CPSF-73 and Dhp1/XRN2 nucleases, supporting widespread cleavage-dependent transcription termination in fission yeast. Our findings thus reveal that a common mode of transcription termination can produce functionally and structurally distinct types of polyadenylated and non-polyadenylated RNAs.
Highlights
Termination of RNA polymerase II (RNAPII) transcription is a fundamental step of gene expression that is critical for determining the borders between genes
We find that mRNA 3′ end processing factors are enriched at the 3′ end of ncRNA genes and that this recruitment coincides with high levels of Ser[2] and Tyr[1] carboxy-terminal domain (CTD) phosphorylation
We previously uncovered a polyadenylation-dependent pathway required for the maturation of independently transcribed small nucleolar RNAs (snoRNAs) that relies on Pab[227,28]
Summary
Termination of RNA polymerase II (RNAPII) transcription is a fundamental step of gene expression that is critical for determining the borders between genes. In S. cerevisiae, transcription of snoRNAs, snRNAs, and CUTs does not rely on the cleavage/polyadenylation machinery for termination, but instead uses a cleavage-independent termination pathway that requires a complex (referred to as NNS complex) consisting of the RNA-binding proteins Nab[3] and Nrd[1] as well as the DNA/RNA helicase Sen[12] In this mode of termination, the NNS complex interacts with both the transcription machinery[9,10] and specific RNA motifs enriched downstream of ncRNA genes[11,12] to engage the transcription elongation complex via the Sen[1] helicase, which translocate onto the nascent RNA and catches up with the transcribing polymerase to elicit termination[13]. Our findings indicate that torpedo-mediated transcription termination is widespread in fission yeast, thereby revealing that a universal mode of transcription termination can promote the synthesis and accumulation of both polyadenylated mRNAs and nonpolyadenylated ncRNAs
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