Selection-driven cost-efficiency optimisation of transcripts modulates gene evolutionary rate in bacteria

2017

Preprint

Self Cite

Background: Genome and transcript sequences are composed of long strings of nucleotide monomers (A, C, G and T/U) that require different quantities of nitrogen atoms for biosynthesis. Results:Here it is shown that the strength of selection acting on transcript nitrogen content is determined by the amount of nitrogen plants require to conduct photosynthesis. Specifically, plants that require more nitrogen to conduct photosynthesis experience stronger selection on transcript sequences to use synonymous codons that cost less nitrogen to biosynthesise. It is further shown that the strength of selection acting on transcript nitrogen cost constrains molecular sequence evolution such that genes experiencing stronger selection evolve at a slower rate. Conclusions:Together these findings reveal that the plant molecular clock is set by photosynthetic efficiency, and provide a mechanistic explanation for changes in plant speciation

Section: Variation In Photosynthetic Nitrogen Use Efficiency Causes Amentioning

confidence: 99%

Section: Variation In the Strength Of Selection Acting On Nitrogen Bimentioning

confidence: 99%

Section: Variation In the Strength Of Selection Acting On Nitrogen Bimentioning

confidence: 99%

Section: Variation In the Strength Of Selection Acting On Nitrogen Bimentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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The amount of nitrogen used for photosynthesis governs molecular evolution in plants

2017

Preprint

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The Amount of Nitrogen Used for Photosynthesis Modulates Molecular Evolution in Plants

Molecular Biology and Evolution

2018

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Genome and transcript sequences are composed of long strings of nucleotide monomers (A, C, G, and T/U) that require different quantities of nitrogen atoms for biosynthesis. Here, it is shown that the strength of selection acting on transcript nitrogen content is influenced by the amount of nitrogen plants require to conduct photosynthesis. Specifically, plants that require more nitrogen to conduct photosynthesis experience stronger selection on transcript sequences to use synonymous codons that cost less nitrogen to biosynthesize. It is further shown that the strength of selection acting on transcript nitrogen cost constrains molecular sequence evolution such that genes experiencing stronger selection evolve at a slower rate. Together these findings reveal that the plant molecular clock is set by photosynthetic efficiency, and provide a mechanistic explanation for changes in plant speciation rates that occur concomitant with improvements in photosynthetic efficiency and changes in the environment such as light, temperature, and atmospheric CO2 concentration.

Selection-driven cost-efficiency optimization of transcripts modulates gene evolutionary rate in bacteria

Seward

2018

Genome Biol

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BackgroundMost amino acids are encoded by multiple synonymous codons. However, synonymous codons are not used equally, and this biased codon use varies between different organisms. It has previously been shown that both selection acting to increase codon translational efficiency and selection acting to decrease codon biosynthetic cost contribute to differences in codon bias. However, it is unknown how these two factors interact or how they affect molecular sequence evolution.ResultsThrough analysis of 1320 bacterial genomes, we show that bacterial genes are subject to multi-objective selection-driven optimization of codon use. Here, selection acts to simultaneously decrease transcript biosynthetic cost and increase transcript translational efficiency, with highly expressed genes under the greatest selection. This optimization is not simply a consequence of the more translationally efficient codons being less expensive to synthesize. Instead, we show that transfer RNA gene copy number alters the cost-efficiency trade-off of synonymous codons such that, for many species, selection acting on transcript biosynthetic cost and translational efficiency act in opposition. Finally, we show that genes highly optimized to reduce cost and increase efficiency show reduced rates of synonymous and non-synonymous mutation.ConclusionsThis analysis provides a simple mechanistic explanation for variation in evolutionary rate between genes that depends on selection-driven cost-efficiency optimization of the transcript. These findings reveal how optimization of resource allocation to messenger RNA synthesis is a critical factor that determines both the evolution and composition of genes.Electronic supplementary materialThe online version of this article (10.1186/s13059-018-1480-7) contains supplementary material, which is available to authorized users.