Nucleolar Pol II interactome reveals TBPL1, PAF1, and Pol I at intergenic rDNA drive rRNA biogenesis

Negin Khosraviani, V. Talya Yerlici, Jonathan St-Germain, Yi Yang Hou, Shi Bo Cao, Carla Ghali, Michael Bokros, Rehna Krishnan, Razqallah Hakem, Stephen Lee, Brian Raught and Karim Mekhail ()
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Negin Khosraviani: University of Toronto
V. Talya Yerlici: University of Toronto
Jonathan St-Germain: University Health Network
Yi Yang Hou: University of Toronto
Shi Bo Cao: University of Toronto
Carla Ghali: University of Toronto
Michael Bokros: University of Miami
Rehna Krishnan: University Health Network
Razqallah Hakem: University Health Network
Stephen Lee: University of Miami
Brian Raught: University Health Network
Karim Mekhail: University of Toronto

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Ribosomal DNA (rDNA) repeats harbor ribosomal RNA (rRNA) genes and intergenic spacers (IGS). RNA polymerase (Pol) I transcribes rRNA genes yielding rRNA components of ribosomes. IGS-associated Pol II prevents Pol I from excessively synthesizing IGS non-coding RNAs (ncRNAs) that can disrupt nucleoli and rRNA production. Here, compartment-enriched proximity-dependent biotin identification (compBioID) revealed the TATA-less-promoter-binding TBPL1 and transcription-regulatory PAF1 with nucleolar Pol II. TBPL1 localizes to TCT motifs, driving Pol II and Pol I and maintaining its baseline ncRNA levels. PAF1 promotes Pol II elongation, preventing unscheduled R-loops that hyper-restrain IGS Pol I-associated ncRNAs. PAF1 or TBPL1 deficiency disrupts nucleolar organization and rRNA biogenesis. In PAF1-deficient cells, repressing unscheduled IGS R-loops rescues nucleolar organization and rRNA production. Depleting IGS Pol I-dependent ncRNAs is sufficient to compromise nucleoli. We present the nucleolar interactome of Pol II and show that its regulation by TBPL1 and PAF1 ensures IGS Pol I ncRNAs maintaining nucleolar structure and function.

Date: 2024
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DOI: 10.1038/s41467-024-54002-w

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