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Niedner, A. ; Monecke, T.* ; Hennig, J. ; Klostermann, M.* ; Hofweber, M.* ; Davydova, E.-O. ; Gerber, A.P.* ; Anosova, I. ; Mayer, W.* ; Müller, M. ; Heym, R.G. ; Janowski, R. ; Paillart, J.C.* ; Dormann, D.* ; Zarnack, K.* ; Sattler, M. ; Niessing, D.

Intrinsically disordered RNA-binding motifs cooperate to catalyze RNA folding and drive phase separation.

Nucleic Acids Res. 52, 14205-14228 (2024)

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RNA-binding proteins are essential for gene regulation and the spatial organization of cells. Here, we report that the yeast ribosome biogenesis factor Loc1p is an intrinsically disordered RNA-binding protein with eight repeating positively charged, unstructured nucleic acid binding (PUN) motifs. While a single of these previously undefined motifs stabilizes folded RNAs, multiple copies strongly cooperate to catalyze RNA folding. In the presence of RNA, these multivalent PUN motifs drive phase separation. Proteome-wide searches in pro- and eukaryotes for proteins with similar arrays of PUN motifs reveal a strong enrichment in RNA-mediated processes and DNA remodeling. Thus, PUN motifs are potentially involved in a large variety of RNA- and DNA-related processes by concentrating them in membraneless organelles. The general function and wide distribution of PUN motifs across species suggest that in an ancient 'RNA world' PUN-like motifs may have supported the correct folding of early ribozymes.

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