Rice Yellow Mottle Virus , an RNA Plant Virus, Evolves as Rapidly as Most RNA Animal Viruses

Abstract

The rate of evolution of an RNA plant virus has never been estimated using temporally spaced sequence data, by contrast to the information available on an increasing range of animal viruses. Accordingly, the evolution rate of Rice yellow mottle virus (RYMV) was calculated from sequences of the coat protein gene of isolates collected from rice over a 40-year period in different parts of Africa. The evolution rate of RYMV was estimated by pairwise distance linear regression on five phylogeographically defined groups comprising a total of 135 isolates. It was further assessed from 253 isolates collected all over Africa by Bayesian coalescent methods under strict and relaxed molecular clock models and under constant size and skyline population genetic models. Consistent estimates of the evolution rate between 4 ؋ 10 ؊4 and 8 ؋ 10 ؊4 nucleotides (nt)/site/year were obtained whatever method and model were applied. The synonymous evolution rate was between 8 ؋ 10 ؊4 and 11 ؋ 10 ؊4 nt/site/year. The overall and synonymous evolution rates of RYMV were within the range of the rates of 50 RNA animal viruses, below the average but above the distribution median. Experimentally, in host change studies, substitutions accumulated at an even higher rate. The results show that an RNA plant virus such as RYMV evolves as rapidly as most RNA animal viruses. Knowledge of the molecular clock of plant viruses provides methods for testing a wide range of biological hypotheses.The mutation rates of RNA viruses (i.e., the number of nucleotide misincorporations per site and per round of replication) are 10 4 to 10 5 times higher than those of their DNA hosts (8, 9). Such a high mutation rate is attributed to the lack of repair function of the RNA polymerase of these viruses, the short replication times, and the large populations in infected hosts (7). A high mutation rate often results in rapid evolution of RNA animal viruses. This allowed the measure of the evolution rates of an extensive range of animal viruses through the analysis of heterochronous sequences, i.e., sequences of viral genes isolated at different times (11,36). A large variation in the evolution rates of RNA animal viruses was subsequently found and was attributed mostly to differences in replication rates (24,26). Estimates of evolution rates are used increasingly to date the emergence and to reconstruct the population dynamics of major viral epidemics (6).Interestingly, some RNA viruses change little or not at all over time. The best-documented example is an RNA plant virus, Tobacco mild green mosaic virus, which showed no increase in genetic diversity over the 90 years considered, in the longest series of isolates with known isolation times for any virus (20). Indeed, many studies have shown the remarkable genetic stability of RNA plant virus populations from different geographical regions, hosts, and collection times (21). It was claimed that most tobamovirus populations are very stable and do not evolve at a measurable rate (22). It was even observed that populations...

Genetic Variation and Possible Mechanisms Driving the Evolution of Worldwide Fig mosaic virus Isolates

“…In California, nucleotide diversity of Cucumber mosaic virus, CTV, and Citrus psorosis virus have been estimated as ≈0. 030 (31,34,46), which is also low in comparison with bacteriophages, animal viruses, and some plant viruses (14,20).…”

“…In California, nucleotide diversity of Cucumber mosaic virus, CTV, and Citrus psorosis virus have been estimated as ≈0. 030 (31,34,46), which is also low in comparison with bacteriophages, animal viruses, and some plant viruses (14,20).Genetic differentiation was evaluated with the statistical tests Ks*, Z*, and S nn , and the extent of genetic differentiation and, therefore, gene flow was estimated with the coefficient F st . When samples collected from the USDA Germplasm collection (located at UC Davis) were compared with the isolates collected from commercial fields in California, the F st value was equal to -0.021 and the three statistical tests were nonsignificant.…”

Time - the emerging dimension of plant virus studies

“…species of the Luteoviridae), 9000 years ago; potyviruses, 6600 years ago; sobemoviruses, 3000 years ago; and the TYLCVs, which are probably representative of the begomoviruses, 10 000 years ago. Thus, these major taxa of crop-infecting viruses all diversified in the period since humankind invented agriculture (Fargette et al, 2008b;Gibbs et al, 2008c) although, of course, they may have originated even earlier and survived as small founder populations. This raises the question as to whether the invention and spread of agriculture itself triggered and fostered their radiation and dominance.…”

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

“…In the case of plant RNA viruses, 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).…”