Academic journal article Genetics

The Rate and Spectrum of Spontaneous Mutations in a Plant RNA Virus

Academic journal article Genetics

The Rate and Spectrum of Spontaneous Mutations in a Plant RNA Virus

Article excerpt

ABSTRACT

Knowing mutation rates and the molecular spectrum of spontaneous mutations is important to understanding how the genetic composition of viral populations evolves. Previous studies have shown that the rate of spontaneous mutations for RNA viruses widely varies between 0.01 and 2 mutations per genome and generation, with plant RNA viruses always occupying the lower side of this range. However, this peculiarity of plant RNA viruses is based on a very limited number of studies. Here we analyze the spontaneous mutational spectrum and the mutation rate of Tobacco etch potyvirus, a model system of positive sense RNA viruses. Our experimental setup minimizes the action of purifying selection on the mutational spectrum, thus giving a picture of what types of mutations are produced by the viral replicase. As expected for a neutral target, we found that transitions and nonsynonymous (including a few stop codons and small deletions) mutations were the most abundant type. This spectrum was notably different from the one previously described for another plant virus. We have estimated that the spontaneous mutation rate for this virus was in the range 10^sup -6^-10^sup -5^ mutations per site and generation. Our estimates are in the same biological ballpark that previous values reported for plant RNA viruses. This finding gives further support to the idea that plant RNA viruses may have lower mutation rates than their animal counterparts.

(ProQuest: ... denotes formulae omitted.)

THE rate of spontaneousmutation is a key parameter to understanding the genetic structure of populations over time. Mutation represents the primary source of genetic variation on which natural selection and genetic drift operate. Although the exact value of the mutation rate is important for several evolutionary theories, accurate estimates are available only for a handful of organisms. RNA viruses show mutation rates that are orders of magnitude higher than those of their DNA-based hosts and in the range of 0.03-2 per genome and replication round (Drake et al. 1998; Drake and Holland 1999; Chao et al. 2002). This difference results from the lack of proofreading activity of the virusencodedRNA- dependentRNApolymerases(Steinhauer et al. 1992). The evolutionary causes of such elevated mutation rates remain unknown and it is commonly accepted that they may be beneficial as a mechanism to escape from the strong selective pressures imposed by the host's defensemechanisms, although not necessarily evolved in response to natural selection (Elena and Sanjuán 2005; Clune et al. 2008). Indeed, in the short term, a too high mutation rate has pernicious effects on viral fitness since most of the mutations produced are deleterious (Bonhoeffer et al. 2004; Sanjuán et al. 2004).

In the case of plantRNAviruses, it has been repeatedly reported that their populations are highly genetically stable (Rodríguez-Cerezo et al. 1991; Fraile et al. 1997; Marco and Aranda 2005; Herránz et al. 2008) in comparison with their animal counterparts, although reports of higher substitution rates also exist (Fargette et al. 2008; Gibbs et al. 2008). This peculiar behavior might be due in part to stronger stabilizing selection, weaker immune-mediated positive selection (García- Arenal et al. 2001), the existence of strong bottlenecks during cell-to-cell movement and systemic colonization of distal tissues (Hall et al. 2001; Sacristán et al. 2003; Li and Roossinck 2004), severe bottlenecks during vector-mediated transmission (Ali et al. 2006; Moury et al. 2007; Betancourt et al. 2008), or differences in the replication mode compared to lytic animal viruses (French and Stenger 2003; Sardanyés et al. 2009). Another more obvious possibility is that, indeed, plant viruses have lower mutation rates than other RNA viruses. Indeed the only two available direct estimates of mutation rates for plant viruses are both in the lower side of the range usually accepted for animal riboviruses: 0. …

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