Polyamines and flg22 reshape the ribosomal protein composition of actively translating ribosomes in plants

Ester Murillo; Federico Martínez-Seidel; Kostadin E. Atanasov; Dione Gentry-Torfer; Alexandre Augusto Pereira Firmino; Alexander Erban; Shuai Nie; Michael G. Leeming; Pipob Suwanchaikasem; Berin A. Boughton; Nicholas A. Williamson; Ute Roessner; Joachim Kopka; Rubén Alcázar

doi:10.1016/j.plaphy.2025.109585

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Polyamines and flg22 reshape the ribosomal protein composition of actively translating ribosomes in plants

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Polyamines and flg22 reshape the ribosomal protein composition of actively translating ribosomes in plants

Ester Murillo, Federico Martínez-Seidel, Kostadin E. Atanasov, Dione Gentry-Torfer, Alexandre Augusto Pereira Firmino, Alexander Erban, Shuai Nie, Michael G. Leeming, Pipob Suwanchaikasem, Berin A. Boughton, …

Plant physiology and biochemistry, Vol.220, 109585

2025

DOI: https://doi.org/10.1016/j.plaphy.2025.109585

PMID: 39893946

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Abstract

flg22

PAMPs

Putrescine

Ribosomes

Spermine

Translation

Polyamines are small, polycationic molecules with amino groups that are present in most living organisms. Studies indicate that polyamines increase general protein synthesis and are essential for efficient translation. While progress has been made in understanding the role of polyamines in translation in bacteria and mammals, their contribution and mode of action in plants remain largely unexplored. In a previous study, we found that putrescine (Put) and the pathogen-associated molecular pattern (PAMP) from bacterial flagellin (flg22) transcriptionally induced ribosome biogenesis in plants. Here we examined the impact of polyamines (Put and spermine, Spm) and flg22 on ribosome complex formation in Arabidopsis. Our results indicate that polyamines, flg22 and their combinations increase the abundance of actively translating polysomes. Riboproteomic analyses revealed that polyamines and flg22 trigger differential changes in the accumulation of ribosomal proteins, which are structurally confined in response to Put. Importantly, Put was found binding to non-translating and actively translating ribosomes, suggesting that this polyamine has a role in functional aspects of translation, such as stabilization and/or remodeling of polysomal complexes. Additional global proteomics analyses in polyamine biosynthesis mutants revealed that lower Put availability triggers changes in proteins associated with ribonucleoprotein complex binding and biogenesis. Overall, our findings highlight the effect of polyamines and flg22 on shaping the ribosomal protein composition of actively translating ribosomes in plants. [Display omitted] •Put, Spm, and their combinations with flg22 increase the abundance of actively translating polysomes.•Polyamines and flg22 reshape protein composition of translating polysomes.•Put triggered changes of ribosomal proteins are structurally confined within 40S subunit complexes.•Put preferentially binds to actively translational ribosome complexes.•Put deficiency alters the proteome and enriches for ribonucleoprotein binding proteins.

Details

Title: Polyamines and flg22 reshape the ribosomal protein composition of actively translating ribosomes in plants
Authors/Creators: Ester Murillo - Universitat de Barcelona
Federico Martínez-Seidel - The University of Melbourne
Kostadin E. Atanasov - Universitat de Barcelona
Dione Gentry-Torfer - Max Planck Institute of Molecular Plant Physiology
Alexandre Augusto Pereira Firmino - Max Planck Institute of Molecular Plant Physiology
Alexander Erban - Max Planck Institute of Molecular Plant Physiology
Shuai Nie - The University of Melbourne
Michael G. Leeming - The University of Melbourne
Pipob Suwanchaikasem - The University of Melbourne
Berin A. Boughton - Murdoch University
Nicholas A. Williamson - The University of Melbourne
Ute Roessner - Australian National University
Joachim Kopka - Max Planck Institute of Molecular Plant Physiology
Rubén Alcázar - Universitat de Barcelona
Publication Details: Plant physiology and biochemistry, Vol.220, 109585
Publisher: Elsevier Masson SAS
Number of pages: 11
Grant note: European Social Fund Investing in your future": PRE2018-083289, MICIU/AEI/10.13039/501100011033
This work was financially supported by the grants: PID2021-126896OB-I00 funded by MICIU/AEI/10.13039/501100011033 (Spain) and by the "European Regional Development Fund (ERDF) a way of making Europe"; PDC2021-121267-I00 funded by MICIU/AEI/10.13039/501100011033 (Spain) and European Union NextGenerationEU/PRTR. E.M. is holder of the grant PRE2018-083289 funded by MICIU/AEI/10.13039/501100011033 and by "European Social Fund Investing in your future".
Identifiers: 991005741585707891
Murdoch Affiliation: Australian National Phenome Centre
Language: English
Resource Type: Journal article

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Collaboration types: Domestic collaboration; International collaboration
Citation topics: 1 Clinical & Life Sciences; 1.320 Molecular & Cell Biology - Polyamines & Paraquat; 1.320.1324 Polyamines
Web Of Science research areas: Plant Sciences
ESI research areas: Plant & Animal Science