Ribosome heterogeneity in Drosophila melanogaster gonads through paralog-switching

Hopes, Tayah; Norris, Karl; Agapiou, Michaela; McCarthy, Charley G.P.; Lewis, Philip A.; O'Connell, Mary J.; Fontana, Juan; Aspden, Julie L.

Abstract

Ribosomes have long been thought of as homogeneous macromolecular machines, but recent evidence suggests they are heterogeneous and could be specialised to regulate translation. Here, we have characterised ribosomal protein heterogeneity across 4 tissues of Drosophila melanogaster. We find that testes and ovaries contain the most heterogeneous ribosome populations, which occurs through a combination of paralog-enrichment and paralog-switching. We have solved structures of ribosomes purified from in vivo tissues by cryo-EM, revealing differences in precise ribosomal arrangement for testis and ovary 80S ribosomes. Differences in the amino acid composition of paralog pairs and their localisation on the ribosome exterior indicate paralog-switching could alter the ribosome surface, enabling different proteins to regulate translation. One testis-specific paralog-switching pair is also found in humans, suggesting this is a conserved site of ribosome heterogeneity. Overall, this work allows us to propose that mRNA translation might be regulated in the gonads through ribosome heterogeneity, providing a potential means of ribosome specialisation.

• Journal Article Type: Article
• Acceptance Date: Jul 2, 2021
• Online Publication Date: Jul 20, 2021
• Publication Date: Feb 28, 2022
• Deposit Date: Nov 28, 2022
• Publicly Available Date: Nov 29, 2022
• Journal: Nucleic Acids Research
• Print ISSN: 0305-1048
• Electronic ISSN: 1362-4962
• Peer Reviewed: Peer Reviewed
• Volume: 50
• Issue: 4
• Pages: 2240-2257
• DOI: https://doi.org/10.1093/nar/gkab606
• Public URL: https://nottingham-repository.worktribe.com/output/7684294
• Publisher URL: https://academic.oup.com/nar/article/50/4/2240/6324614