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Why genes overlap in viruses.

Chirico N, Vianelli A, Belshaw R - Proc. Biol. Sci. (2010)

Bottom Line: We conclude that gene overlap is unlikely to have evolved as a way of compressing the genome in response to the harmful effect of mutation because RNA viruses, despite having generally higher mutation rates, have less gene overlap on average than DNA viruses of comparable genome length.Our interpretation is that a physical constraint on genome length by the capsid has led to gene overlap evolving as a mechanism for producing more proteins from the same genome length.We consider that these patterns cannot be explained by other factors, namely the possible roles of overlap in transcription regulation, generating more divergent proteins and the relationship between gene length and genome length.

View Article: PubMed Central - PubMed

Affiliation: Department of Structural and Functional Biology, University of Insubria, Via JH Dunant 3, 21100 Varese, Italy.

ABSTRACT
The genomes of most virus species have overlapping genes--two or more proteins coded for by the same nucleotide sequence. Several explanations have been proposed for the evolution of this phenomenon, and we test these by comparing the amount of gene overlap in all known virus species. We conclude that gene overlap is unlikely to have evolved as a way of compressing the genome in response to the harmful effect of mutation because RNA viruses, despite having generally higher mutation rates, have less gene overlap on average than DNA viruses of comparable genome length. However, we do find a negative relationship between overlap proportion and genome length among viruses with icosahedral capsids, but not among those with other capsid types that we consider easier to enlarge in size. Our interpretation is that a physical constraint on genome length by the capsid has led to gene overlap evolving as a mechanism for producing more proteins from the same genome length. We consider that these patterns cannot be explained by other factors, namely the possible roles of overlap in transcription regulation, generating more divergent proteins and the relationship between gene length and genome length.

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Predicted capsid volume increases in moving up to the nearest available T number compared with genome length for some DNA viruses. For further details see §2.
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RSPB20101052F1: Predicted capsid volume increases in moving up to the nearest available T number compared with genome length for some DNA viruses. For further details see §2.

Mentions: Many viruses have capsids that are icosahedral (20 sided), varying in the number of protein units (capsomers) that form each side. In such viruses, an increase in capsid size is generally achieved through increases in the number rather than the size of these capsomers (Rossmann & Erickson 1985; Chapman & Liljas 2003; Shepherd & Reddy 2005; Krupovic & Bamford 2008). These increases in capsomer number are in discrete steps following a geometric pattern represented by the so-called T (Triangulation) number series (Caspar & Klug 1962), which appears to be thermodynamically determined (Zandi et al. 2004). As the T values increase, the differences in volume (as a percentage) between adjacent T numbers become smaller, with the product of the capsid diameter and the reciprocal of the square root of T remaining constant (Walker & Anderson 1970; Rossmann & Erickson 1985; Hu et al. 2008). The actual pattern of historical transitions between different T numbers is unknown and probably determined by the type of fold found in the capsomer (Ahlquist 2005; Bamford et al. 2005; Krupovic & Bamford 2008). We discuss this in the electronic supplementary material. In figure 1, we illustrate the general principle using some DNA viruses, chosen because both their T number is known, and because of capsomer fold similarity, we can infer the likely next highest possible T number.Figure 1.


Why genes overlap in viruses.

Chirico N, Vianelli A, Belshaw R - Proc. Biol. Sci. (2010)

Predicted capsid volume increases in moving up to the nearest available T number compared with genome length for some DNA viruses. For further details see §2.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2992710&req=5

RSPB20101052F1: Predicted capsid volume increases in moving up to the nearest available T number compared with genome length for some DNA viruses. For further details see §2.
Mentions: Many viruses have capsids that are icosahedral (20 sided), varying in the number of protein units (capsomers) that form each side. In such viruses, an increase in capsid size is generally achieved through increases in the number rather than the size of these capsomers (Rossmann & Erickson 1985; Chapman & Liljas 2003; Shepherd & Reddy 2005; Krupovic & Bamford 2008). These increases in capsomer number are in discrete steps following a geometric pattern represented by the so-called T (Triangulation) number series (Caspar & Klug 1962), which appears to be thermodynamically determined (Zandi et al. 2004). As the T values increase, the differences in volume (as a percentage) between adjacent T numbers become smaller, with the product of the capsid diameter and the reciprocal of the square root of T remaining constant (Walker & Anderson 1970; Rossmann & Erickson 1985; Hu et al. 2008). The actual pattern of historical transitions between different T numbers is unknown and probably determined by the type of fold found in the capsomer (Ahlquist 2005; Bamford et al. 2005; Krupovic & Bamford 2008). We discuss this in the electronic supplementary material. In figure 1, we illustrate the general principle using some DNA viruses, chosen because both their T number is known, and because of capsomer fold similarity, we can infer the likely next highest possible T number.Figure 1.

Bottom Line: We conclude that gene overlap is unlikely to have evolved as a way of compressing the genome in response to the harmful effect of mutation because RNA viruses, despite having generally higher mutation rates, have less gene overlap on average than DNA viruses of comparable genome length.Our interpretation is that a physical constraint on genome length by the capsid has led to gene overlap evolving as a mechanism for producing more proteins from the same genome length.We consider that these patterns cannot be explained by other factors, namely the possible roles of overlap in transcription regulation, generating more divergent proteins and the relationship between gene length and genome length.

View Article: PubMed Central - PubMed

Affiliation: Department of Structural and Functional Biology, University of Insubria, Via JH Dunant 3, 21100 Varese, Italy.

ABSTRACT
The genomes of most virus species have overlapping genes--two or more proteins coded for by the same nucleotide sequence. Several explanations have been proposed for the evolution of this phenomenon, and we test these by comparing the amount of gene overlap in all known virus species. We conclude that gene overlap is unlikely to have evolved as a way of compressing the genome in response to the harmful effect of mutation because RNA viruses, despite having generally higher mutation rates, have less gene overlap on average than DNA viruses of comparable genome length. However, we do find a negative relationship between overlap proportion and genome length among viruses with icosahedral capsids, but not among those with other capsid types that we consider easier to enlarge in size. Our interpretation is that a physical constraint on genome length by the capsid has led to gene overlap evolving as a mechanism for producing more proteins from the same genome length. We consider that these patterns cannot be explained by other factors, namely the possible roles of overlap in transcription regulation, generating more divergent proteins and the relationship between gene length and genome length.

Show MeSH
Related in: MedlinePlus