The role of codon selection in regulation of translation efficiency deduced from synthetic libraries

Navon, Sivan; Pilpel, Yitzhak

doi:10.1186/gb-2011-12-2-r12

Cited by 38 publications

(45 citation statements)

References 23 publications

(44 reference statements)

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“…The balance between supply and demand, i.e., the extent of adaptation of the tRNA pool to the codon usage in the transcriptome, could affect production levels of proteins (Qian et al, 2012). In addition, cellular fitness could be affected by the extent of a global codon-to-tRNA adaptation (Kudla et al, 2009;Navon and Pilpel, 2011), and especially highly expressed genes appear to be codon optimized (Gingold et al, 2012). It was suggested that low compatibility between demand and supply, especially if presented by highly expressed genes, can result in a global inefficient allocation of resources such as ribosomes and thus could be fitness reducing (Kudla et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation

Gingold

Tehler

Christoffersen

et al. 2014

Cell

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443

498

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A dichotomous choice for metazoan cells is between proliferation and differentiation. Measuring tRNA pools in various cell types, we found two distinct subsets, one that is induced in proliferating cells, and repressed otherwise, and another with the opposite signature. Correspondingly, we found that genes serving cell-autonomous functions and genes involved in multicellularity obey distinct codon usage. Proliferation-induced and differentiation-induced tRNAs often carry anticodons that correspond to the codons enriched among the cell-autonomous and the multicellularity genes, respectively. Because mRNAs of cell-autonomous genes are induced in proliferation and cancer in particular, the concomitant induction of their codon-enriched tRNAs suggests coordination between transcription and translation. Histone modifications indeed change similarly in the vicinity of cell-autonomous genes and their corresponding tRNAs, and in multicellularity genes and their tRNAs, suggesting the existence of transcriptional programs coordinating tRNA supply and demand. Hence, we describe the existence of two distinct translation programs that operate during proliferation and differentiation.

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Section: Introductionmentioning

confidence: 99%

A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation

Gingold

Tehler

Christoffersen

et al. 2014

Cell

Self Cite

443

498

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“…The in vivo rate and accuracy of translation are affected by the use or disuse of “major” codons in Escherichia coli (Tuller et al 2010; Navon and Pilpel 2011), and early observations of genome-wide synonymous codon usage in D. melanogaster and C. elegans showed a bias toward a subset of codons (Shields et al 1988; Stenico et al 1994). This set of preferred codons corresponds to the most abundant tRNAs in the cell and, by proxy, the number of tRNA gene copies in the genome (Moriyama and Powell 1997; Duret 2000).…”

mentioning

confidence: 99%

Genome-Wide Patterns of Codon Bias Are Shaped by Natural Selection in the Purple Sea Urchin,Strongylocentrotus purpuratus

Kober

Pogson

2013

G3 Genes|Genomes|Genetics

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Codon usage bias has been documented in a wide diversity of species, but the relative contributions of mutational bias and various forms of natural selection remain unclear. Here, we describe for the first time genome-wide patterns of codon bias at 4623 genes in the purple sea urchin, Strongylocentrotus purpuratus. Preferred codons were identified at 18 amino acids that exclusively used G or C at third positions, which contrasted with the strong AT bias of the genome (overall GC content is 36.9%). The GC content of third positions and coding regions exhibited significant correlations with the magnitude of codon bias. In contrast, the GC content of introns and flanking regions was indistinguishable from the genome-wide background, which suggested a limited contribution of mutational bias to synonymous codon usage. Five distinct clusters of genes were identified that had significantly different synonymous codon usage patterns. A significant correlation was observed between codon bias and mRNA expression supporting translational selection, but this relationship was driven by only one highly biased cluster that represented only 8.6% of all genes. In all five clusters preferred codons were evolutionarily conserved to a similar degree despite differences in their synonymous codon usage distributions and magnitude of codon bias. The third positions of preferred codons in two codon usage groups also paired significantly more often in stems than in loops of mRNA secondary structure predictions, which suggested that codon bias might also affect mRNA stability. Our results suggest that mutational bias has played a minor role in determining codon bias in S. purpuratus and that preferred codon usage may be heterogeneous across different genes and subject to different forms of natural selection.

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“…Evolutionary traits may have been developed in order to optimally couple the transcription of protein-coding genes and the translation initiation of mRNA in prokaryotes. A ramp of hydrogen bonding can be one such trait that optimizes transcription efficiency at the 5 -end of CDSs so that transcription can be efficiently coupled with a ramp of translation efficiency found also at the 5 -end of CDSs 11,35,36 . Although both transcription and translation seem to be mediated by an initial ramp, the ramps have opposite efficiency.…”

Section: Discussionmentioning

confidence: 99%

Codon usage bias creates a ramp of hydrogen bonding at the 5′-end in prokaryotic ORFeomes

Villada

Duran

Lee

2019

Preprint

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Codon usage bias exerts control over a wide variety of molecular processes. The positioning of synonymous codons within coding sequences (CDSs) dictates protein expression by mechanisms such as local translation efficiency, mRNA Gibbs free energy, and protein co-translational folding. In this work, we explore how codon variants affect the position-dependent content of hydrogen bonding, which in turn influences energy requirements for unwinding double-stranded DNA. By analyzing over 14,000 bacterial, archaeal, and fungal ORFeomes, we found that Bacteria and Archaea exhibit an exponential ramp of hydrogen bonding at the 5 -end of CDSs, while a similar ramp was not found in Fungi. The ramp develops within the first 20 codon positions in prokaryotes, eventually reaching a steady carrying capacity of hydrogen bonding that does not differ from Fungi. Selection against uniformity tests proved that selection acts against synonymous codons with high content of hydrogen bonding at the 5 -end of prokaryotic ORFeomes. Overall, this study provides novel insights into the molecular feature of hydrogen bonding that is governed by the genetic code at the 5 -end of CDSs. A web-based application to analyze the position-dependent hydrogen bonding of ORFeomes has been developed and is publicly available (https: //juanvillada.shinyapps.io/hbonds/).

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The role of codon selection in regulation of translation efficiency deduced from synthetic libraries

Cited by 38 publications

References 23 publications

A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation

A Dual Program for Translation Regulation in Cellular Proliferation and Differentiation

Genome-Wide Patterns of Codon Bias Are Shaped by Natural Selection in the Purple Sea Urchin,Strongylocentrotus purpuratus

Codon usage bias creates a ramp of hydrogen bonding at the 5′-end in prokaryotic ORFeomes

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