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

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.