tRNA Maturation Defects Lead to Inhibition of rRNA Processing via Synthesis of pppGpp

Aude Trinquier; Jonathan E Ulmer; Laetitia Gilet; Sabine Figaro; Philippe Hammann; Lauriane Kuhn; Frédérique Braun; Ciarán Condon

doi:10.1016/j.molcel.2019.03.030

tRNA Maturation Defects Lead to Inhibition of rRNA Processing via Synthesis of pppGpp

Mol Cell. 2019 Jun 20;74(6):1227-1238.e3. doi: 10.1016/j.molcel.2019.03.030. Epub 2019 Apr 16.

Authors

Aude Trinquier¹, Jonathan E Ulmer¹, Laetitia Gilet¹, Sabine Figaro¹, Philippe Hammann², Lauriane Kuhn², Frédérique Braun³, Ciarán Condon⁴

Affiliations

¹ UMR8261 (CNRS-Université Paris Diderot), Institut de Biologie Physico-Chimique, 13 rue Pierre et Marie Curie, 75005 Paris, France.
² Plateforme Proteomique Strasbourg - Esplanade, Institut de Biologie Moléculaire et Cellulaire, CNRS FR1589, 15 rue Descartes, 67084 Strasbourg Cedex, France.
³ UMR8261 (CNRS-Université Paris Diderot), Institut de Biologie Physico-Chimique, 13 rue Pierre et Marie Curie, 75005 Paris, France. Electronic address: frederique.braun@ibpc.fr.
⁴ UMR8261 (CNRS-Université Paris Diderot), Institut de Biologie Physico-Chimique, 13 rue Pierre et Marie Curie, 75005 Paris, France. Electronic address: condon@ibpc.fr.

PMID: 31003868
DOI: 10.1016/j.molcel.2019.03.030

Abstract

rRNAs and tRNAs universally require processing from longer primary transcripts to become functional for translation. Here, we describe an unsuspected link between tRNA maturation and the 3' processing of 16S rRNA, a key step in preparing the small ribosomal subunit for interaction with the Shine-Dalgarno sequence in prokaryotic translation initiation. We show that an accumulation of either 5' or 3' immature tRNAs triggers RelA-dependent production of the stringent response alarmone (p)ppGpp in the Gram-positive model organism Bacillus subtilis. The accumulation of (p)ppGpp and accompanying decrease in GTP levels specifically inhibit 16S rRNA 3' maturation. We suggest that cells can exploit this mechanism to sense potential slowdowns in tRNA maturation and adjust rRNA processing accordingly to maintain the appropriate functional balance between these two major components of the translation apparatus.

Keywords: RNA maturation; ppGpp; rRNA; ribosome biogenesis; stringent response; tRNA.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Bacillus subtilis / genetics*
Bacillus subtilis / metabolism
Base Sequence
Gene Expression Regulation, Bacterial*
Guanosine Pentaphosphate / biosynthesis*
Guanosine Pentaphosphate / genetics
Guanosine Triphosphate / metabolism
Ligases / genetics
Ligases / metabolism
Nucleic Acid Conformation
Peptide Chain Initiation, Translational*
RNA, Ribosomal, 16S / chemistry
RNA, Ribosomal, 16S / genetics*
RNA, Ribosomal, 16S / metabolism
RNA, Transfer / chemistry
RNA, Transfer / genetics*
RNA, Transfer / metabolism
Ribosome Subunits, Large, Bacterial / genetics
Ribosome Subunits, Large, Bacterial / metabolism
Ribosome Subunits, Small, Bacterial / genetics
Ribosome Subunits, Small, Bacterial / metabolism

Substances

RNA, Ribosomal, 16S
Guanosine Pentaphosphate
Guanosine Triphosphate
RNA, Transfer
Ligases
guanosine 3',5'-polyphosphate synthetases