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Trade-off between cost and efficiency during mRNA translation is largely driven by natural selection in angiosperms

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Abstract

Synonymous codons are decoded at different rates during translation elongation, presumably due to the differences in tRNA availability. The biosynthetic cost of each synonymous codon might also differ from each other. Lower cost and higher translation efficiency are both favorable, but optimization of both features is rare. In the plant kingdom, whether the cost-efficiency trade-off/dilemma exists remains largely unknown. To address this, we collected nine well-annotated angiosperms plus additional 60 plant species. We investigated the selection patterns of the cost-efficiency trade-off. At both codon and gene level, the biosynthetic cost and translation efficiency are positively correlated. Higher efficiency is achieved at the expense of higher cost. Interestingly, the genes undergoing stronger selection constraint tend to optimize their cost-efficiency balance. In Arabidopsis, optimized genes are enriched in the most conserved and highly expressed genes. Our study demonstrates the presence of cost-efficiency trade-offs in plants and shows how variation in cost and efficiency interplay at codon and gene levels. Our findings could provide novel perspectives for genome evolution in angiosperms.

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Acknowledgements

We thank all members in Wei Lab for their constructive suggestions to this project.

Funding

This research was financially supported by the National Natural Science Foundation of China (Grant no. 31770213). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Contributions

Lai Wei designed and supervised this research. Both Duan Chu and Lai Wei analyzed the data. Lai Wei defined the phylogenetic relationship between the plant species used in this study. Duan Chu calculated the parameters for codon usage bias. Duan Chu and Lai Wei wrote this article.

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Correspondence to Lai Wei.

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The authors declare they have no conflict of interest.

Information on Electronic Supplementary Material

Online Resource 1. Correlation between the amino acid (AA) frequencies in the genome and tRNAs. Each of the 20 dots in the panels represents one of the 20 AAs. Spearman correlation coefficients are shown in the plot.

Online Resource 2. Correlation between the codon level tAI and nitrogen cost. Spearman correlation coefficients are shown in proportion to the red color.

Online Resource 3. Correlation between the gene level tAI and nitrogen cost. Spearman correlation coefficients are shown in the plot.

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Chu, D., Wei, L. Trade-off between cost and efficiency during mRNA translation is largely driven by natural selection in angiosperms. Plant Syst Evol 306, 92 (2020). https://doi.org/10.1007/s00606-020-01721-4

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  • DOI: https://doi.org/10.1007/s00606-020-01721-4

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