Recruitment of bifunctional regulator thermospermine to methylated ribosomes directs xylem fate

Polyamines are often associated with ribosomes and are thought to stabilize their integrity. In <i>Arabidopsis</i>, the polyamine thermospermine (tSpm) affects xylem cell fate. tSpm induces translation of SUPPRESSOR-OF-ACAULIS51 (SAC51) and SAC51-LIKEs (SACLs), which inhibit heterodimerization of the xylem development proteins LONESOME-HIGHWAY (LHW) and TARGET-OF-MONOPTEROS5. Here, we report a methyltransferase, OVERACHIEVER, that methylates the peptidyl transferase center of the 25<i>S</i> ribosomal RNA (rRNA). Residue m<sup>3</sup>U2952 promotes functional tSpm binding to a specific site connecting the P-site transfer RNA (tRNA) with rRNA residues in the peptidyl transferase center. This interaction enhances the translation of SACLs but inhibits that of LHW. Our study uncovers the dependency between a conserved rRNA base methylation and a polyamine in orchestrating cell fate decisions, highlighting a role for the ribosome chemical landscape in translational regulation.

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Journal
Science
Published
2026-02-12
DOI
https://doi.org/10.1126/science.adx2867
Primary Topic
Polyamine Metabolism and Applications
Type
article
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article

Recruitment of bifunctional regulator thermospermine to methylated ribosomes directs xylem fate

Holm Liisa, Rupert G. Fray, Xiaonan Liu, Cristina Úrbez et al.
Science
Polyamine Metabolism and Applications
article

Recruitment of bifunctional regulator thermospermine to methylated ribosomes directs xylem fate

Holm Liisa, Rupert G. Fray, Xiaonan Liu, Cristina Úrbez, Mariia Shcherbii, Gugan Eswaran, Eva Hellmann, Ville O. Paavilainen, Karolina Stefanowicz, Alan J. Warren, Petri Törönen, Finn Kirpekar, Susanne Mandrup, Julia P. Vainonen, Teva Vernoux, Ronni Nielsen, Mikko J. Frilander, Zsuzsanna Bódi, Brecht Wybouw, Donghwi Ko, Maija Sierla, Robert Malinowski, Anja Paatero, Sedeer El‐Showk, Miguel Blázquez, Alexandre Faille, Raili Ruonala, Nuria De Diego, Martin Balcerowicz, Anders Kristian Haakonsson, Fabrice BESNARD, Patrick Perkins, Tiina Öhman, Tanya Waldie, Ari Pekka Mähönen, Anna N. Stepanova, Markku Varjosalo, Kari Salokas, Huili Liu, A. Tormos Ferrando, Sanja Ćavar Zeljković, Ottoline Leyser, Yka Helariutta, Tine Drud Lundager Rasmussen, Matthieu Bourdon, Serina Mazzoni-Putman, Hanna Help, Jose Alonso, Steffen Heber, Ondrej Novak, Karin Ljung, Xiaomin Liu
article en

Abstract

Polyamines are often associated with ribosomes and are thought to stabilize their integrity. In <i>Arabidopsis</i>, the polyamine thermospermine (tSpm) affects xylem cell fate. tSpm induces translation of SUPPRESSOR-OF-ACAULIS51 (SAC51) and SAC51-LIKEs (SACLs), which inhibit heterodimerization of the xylem development proteins LONESOME-HIGHWAY (LHW) and TARGET-OF-MONOPTEROS5. Here, we report a methyltransferase, OVERACHIEVER, that methylates the peptidyl transferase center of the 25<i>S</i> ribosomal RNA (rRNA). Residue m<sup>3</sup>U2952 promotes functional tSpm binding to a specific site connecting the P-site transfer RNA (tRNA) with rRNA residues in the peptidyl transferase center. This interaction enhances the translation of SACLs but inhibits that of LHW. Our study uncovers the dependency between a conserved rRNA base methylation and a polyamine in orchestrating cell fate decisions, highlighting a role for the ribosome chemical landscape in translational regulation.

ScienceVol. 391(6786)
Université Claude Bernard Lyon 1 (FR), South China Agricultural University (CN), École Normale Supérieure de Lyon (FR), Centre National de la Recherche Scientifique (FR), University of Helsinki (FI), North Carolina State University (US), University of Nottingham (GB), University of Dundee (GB), University of Southern Denmark (DK), Wellcome/MRC Cambridge Stem Cell Institute (GB), University of Cambridge (GB), Sainsbury Laboratory (GB), Swedish University of Agricultural Sciences (SE), Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR), Regional Centre of Advanced Technologies and Materials (CZ), Umeå Plant Science Centre (SE), Laboratoire Reproduction et Développement des Plantes (FR), Institute of Plant Genetics, Polish Academy of Sciences (PL), Czech Academy of Sciences, Institute of Experimental Botany (CZ), Instituto de Biología Molecular y Celular de Plantas (ES), University of Tartu (EE), Palacký University Olomouc (CZ), Polish Academy of Sciences (PL)
Openalex Percentile: Top 59%
Polyamine Metabolism and Applications
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