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Codon and Amino Acid Usage Are Shaped by Selection Across Divergent Model Organisms of the Pancrustacea.

Whittle CA, Extavour CG - G3 (Bethesda) (2015)

Bottom Line: We report strong signals of AT3 optimal codons (those favored in highly expressed genes) in G. bimaculatus and O. fasciatus, whereas weaker signs of GC3 optimal codons were found in P. hawaiensis, suggesting selection on codon usage in all three organisms.Further, in G. bimaculatus and O. fasciatus, high expression was associated with lowered frequency of amino acids with large size/complexity (S/C) scores in favor of those with intermediate S/C values; thus, selection may favor smaller amino acids while retaining those of moderate size for protein stability or conformation.Together, based on examination of 1,680,067, 1,667,783, and 1,326,896 codon sites in G. bimaculatus, O. fasciatus, and P. hawaiensis, respectively, we conclude that translational selection shapes codon and amino acid usage in these three Pancrustacean arthropods.

View Article: PubMed Central - PubMed

Affiliation: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138.

No MeSH data available.


The average frequency of optimal codons (Fop) relative to expression level for the three species of invertebrates. Expression of coding sequence was categorized as low (above 95th percentile), moderate (between 5th and 95th percentile), and high (below 5th percentile). Error bars represent standard errors and are very small.
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fig2: The average frequency of optimal codons (Fop) relative to expression level for the three species of invertebrates. Expression of coding sequence was categorized as low (above 95th percentile), moderate (between 5th and 95th percentile), and high (below 5th percentile). Error bars represent standard errors and are very small.

Mentions: Using the optimal codon lists in Table 1, we calculated the frequency of optimal codons (Fop) (Ikemura 1981) for each CDS under study and found that this parameter was highly statistically significantly and positively correlated to RPM across all CDS for G. bimaculatus (Spearman Rank R = 0.23, P < 10−15), O. fasciatus (R = 0.17, P < 10−15), and P. hawaiensis (R = 0.09, P < 10−15). The R values were each <0.3, suggesting a moderate, yet highly significant, association between Fop and RPM. We subsequently binned each CDS into one of three distinct RPM categories, namely low (below the 5th percentile), moderate (between the 5th and the 95th percentile), and high (above the 95th percentile). This approach revealed an unambiguous shift in Fop, increasing progressively from the low, moderate to high RPM classes for G. bimaculatus, O. fasciatus, and P. hawaiensis (Figure 2), a trend consistent with a strong connection between transcription rates and Fop. Thus, although selection on codon usage has greatest effects in the uppermost expression levels, it also shapes codon usage (albeit to a lesser extent) in moderately expressed genes in those taxa. The weakest effect appears to be for moderately expressed genes in P. hawaiensis, which was only modestly higher than the low expression class. Thus, optimization of codon usage for the moderate expression level classes may be mild in this taxon given the relatively low absolute value of the genome-wide R value above, the similarity of Fop to the lowest class (Figure 2), and the fact that ENC showed an effect only in the highest expression category (see Identification of optimal codons). Given these trends, it is evident that the method of contrasting of expression among the CDS with the 5% highest and lowest RPM used herein, was advantageous in revealing the list of optimal codons. This agrees with prior research indicating that comparison of codon usage among the highest and lowest expressed CDS (known as the comparison method) provides a more effective tool (not weakened by mild correlations in the mid-ranges of expression) for revealing optimal codons than broad correlations between codon usage and expression across all CDS (known as the correlation method), at least for these particular organisms (Hershberg and Petrov 2009; Wang et al. 2011).


Codon and Amino Acid Usage Are Shaped by Selection Across Divergent Model Organisms of the Pancrustacea.

Whittle CA, Extavour CG - G3 (Bethesda) (2015)

The average frequency of optimal codons (Fop) relative to expression level for the three species of invertebrates. Expression of coding sequence was categorized as low (above 95th percentile), moderate (between 5th and 95th percentile), and high (below 5th percentile). Error bars represent standard errors and are very small.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4632051&req=5

fig2: The average frequency of optimal codons (Fop) relative to expression level for the three species of invertebrates. Expression of coding sequence was categorized as low (above 95th percentile), moderate (between 5th and 95th percentile), and high (below 5th percentile). Error bars represent standard errors and are very small.
Mentions: Using the optimal codon lists in Table 1, we calculated the frequency of optimal codons (Fop) (Ikemura 1981) for each CDS under study and found that this parameter was highly statistically significantly and positively correlated to RPM across all CDS for G. bimaculatus (Spearman Rank R = 0.23, P < 10−15), O. fasciatus (R = 0.17, P < 10−15), and P. hawaiensis (R = 0.09, P < 10−15). The R values were each <0.3, suggesting a moderate, yet highly significant, association between Fop and RPM. We subsequently binned each CDS into one of three distinct RPM categories, namely low (below the 5th percentile), moderate (between the 5th and the 95th percentile), and high (above the 95th percentile). This approach revealed an unambiguous shift in Fop, increasing progressively from the low, moderate to high RPM classes for G. bimaculatus, O. fasciatus, and P. hawaiensis (Figure 2), a trend consistent with a strong connection between transcription rates and Fop. Thus, although selection on codon usage has greatest effects in the uppermost expression levels, it also shapes codon usage (albeit to a lesser extent) in moderately expressed genes in those taxa. The weakest effect appears to be for moderately expressed genes in P. hawaiensis, which was only modestly higher than the low expression class. Thus, optimization of codon usage for the moderate expression level classes may be mild in this taxon given the relatively low absolute value of the genome-wide R value above, the similarity of Fop to the lowest class (Figure 2), and the fact that ENC showed an effect only in the highest expression category (see Identification of optimal codons). Given these trends, it is evident that the method of contrasting of expression among the CDS with the 5% highest and lowest RPM used herein, was advantageous in revealing the list of optimal codons. This agrees with prior research indicating that comparison of codon usage among the highest and lowest expressed CDS (known as the comparison method) provides a more effective tool (not weakened by mild correlations in the mid-ranges of expression) for revealing optimal codons than broad correlations between codon usage and expression across all CDS (known as the correlation method), at least for these particular organisms (Hershberg and Petrov 2009; Wang et al. 2011).

Bottom Line: We report strong signals of AT3 optimal codons (those favored in highly expressed genes) in G. bimaculatus and O. fasciatus, whereas weaker signs of GC3 optimal codons were found in P. hawaiensis, suggesting selection on codon usage in all three organisms.Further, in G. bimaculatus and O. fasciatus, high expression was associated with lowered frequency of amino acids with large size/complexity (S/C) scores in favor of those with intermediate S/C values; thus, selection may favor smaller amino acids while retaining those of moderate size for protein stability or conformation.Together, based on examination of 1,680,067, 1,667,783, and 1,326,896 codon sites in G. bimaculatus, O. fasciatus, and P. hawaiensis, respectively, we conclude that translational selection shapes codon and amino acid usage in these three Pancrustacean arthropods.

View Article: PubMed Central - PubMed

Affiliation: Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138.

No MeSH data available.