A higher order PUF complex is central to regulation of C. elegans germline stem cells

Chen Qiu, Sarah L. Crittenden, Brian H. Carrick, Lucas B. Dillard, Stephany J. Costa Dos Santos, Venkata P. Dandey, Robert C. Dutcher, Elizabeth G. Viverette, Robert N. Wine, Jennifer Woodworth, Zachary T. Campbell, Marvin Wickens, Mario J. Borgnia, Judith Kimble () and Traci M. Tanaka Hall ()
Additional contact information
Chen Qiu: National Institutes of Health
Sarah L. Crittenden: University of Wisconsin
Brian H. Carrick: University of Wisconsin
Lucas B. Dillard: National Institutes of Health
Stephany J. Costa Dos Santos: University of Wisconsin
Venkata P. Dandey: National Institutes of Health
Robert C. Dutcher: National Institutes of Health
Elizabeth G. Viverette: National Institutes of Health
Robert N. Wine: National Institutes of Health
Jennifer Woodworth: University of Wisconsin
Zachary T. Campbell: University of Wisconsin School of Medicine and Public Health
Marvin Wickens: University of Wisconsin
Mario J. Borgnia: National Institutes of Health
Judith Kimble: University of Wisconsin
Traci M. Tanaka Hall: National Institutes of Health

Nature Communications, 2025, vol. 16, issue 1, 1-18

Abstract: Abstract PUF RNA-binding proteins are broadly conserved stem cell regulators. Nematode PUF proteins maintain germline stem cells (GSCs) and, with key partner proteins, repress differentiation mRNAs, including gld-1. Here we report that PUF protein FBF-2 and its partner LST-1 form a ternary complex that represses gld-1 via a pair of adjacent FBF binding elements (FBEs) in its 3′UTR. One LST-1 molecule links two FBF-2 molecules via motifs in the LST-1 intrinsically-disordered region; the gld-1 FBE pair includes a well-established ‘canonical’ FBE and a newly-identified noncanonical FBE. Remarkably, this FBE pair drives both full RNA repression in GSCs and full RNA activation upon differentiation. Discoveries of the LST-1–FBF-2 ternary complex, the gld-1 adjacent FBEs, and their in vivo significance predict an expanded regulatory repertoire of different assemblies of PUF-partner-RNA higher order complexes in nematode GSCs. This also suggests analogous PUF controls may await discovery in other biological contexts and organisms.

Date: 2025
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DOI: 10.1038/s41467-024-55526-x

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