The evolution of genome compression and genomic novelty in RNA viruses

Belshaw, Robert; Pybus, Oliver G.; Rambaut, Andrew

doi:10.1101/gr.6305707

Cited by 150 publications

(187 citation statements)

References 47 publications

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“…According to one view, gene overlapping maximizes the genetic information in smaller genomes (1,39). Alternatively, it has been suggested that gene overlap generates mutational robustness (i.e., the ability to preserve phenotypes despite the genomic mutational load) at the population level (2,16,42). Under the latter hypothesis, gene overlapping generates hypersensitivity to deleterious mutations, as these affect more than one gene.…”

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confidence: 99%

Long-Term Evolution of theLuteoviridae: Time Scale and Mode of Virus Speciation

Pagán

Holmes

2010

J Virol

126

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Despite their importance as agents of emerging disease, the time scale and evolutionary processes that shape the appearance of new viral species are largely unknown. To address these issues, we analyzed intra-and interspecific evolutionary processes in the Luteoviridae family of plant RNA viruses. Using the coat protein gene of 12 members of the family, we determined their phylogenetic relationships, rates of nucleotide substitution, times to common ancestry, and patterns of speciation. An associated multigene analysis enabled us to infer the nature of selection pressures and the genomic distribution of recombination events. Although rates of evolutionary change and selection pressures varied among genes and species and were lower in some overlapping gene regions, all fell within the range of those seen in animal RNA viruses. Recombination breakpoints were commonly observed at gene boundaries but less so within genes. Our molecular clock analysis suggested that the origin of the currently circulating Luteoviridae species occurred within the last 4 millennia, with intraspecific genetic diversity arising within the last few hundred years. Speciation within the Luteoviridae may therefore be associated with the expansion of agricultural systems. Finally, our phylogenetic analysis suggested that viral speciation events tended to occur within the same plant host species and country of origin, as expected if speciation is largely sympatric, rather than allopatric, in nature.Although RNA viruses are the most common agents of emerging disease, key aspects of their evolution are still only partly understood. This is of both academic and practical importance, as virus evolution may compromise disease control strategies, including the rapid generation of genotypes that are able to evade host immune responses or of those that are resistant to antivirals or crop genetic resistance (20,34,47).Most of our knowledge of the rapidity of RNA virus evolution comes from the study of animal viruses, for which estimates of rates of nucleotide substitution normally fall within 1 order of magnitude of 1 ϫ 10 Ϫ3 nucleotide substitutions per site per year (subs/site/year) and largely reflect the background mutation rate (10,13,29,37,53). Equivalent studies on plant RNA viruses have reported more heterogeneous rates. Early studies suggested that some plant RNA viruses evolved more slowly than RNA viruses that infect animals. For example, estimates of the nucleotide substitution rate in the range of ϳ1 ϫ 10 Ϫ6 to 1 ϫ 10 Ϫ8 subs/site/year have been obtained for Turnip yellow mosaic virus (4, 23) and some tobamoviruses (21,25). In contrast, more recent estimates using Bayesian coalescent methods applied to sequences with known dates of sampling and allowing for rate variation among lineages have reported substitution rates in the same range as those of animal RNA viruses (22, 63) and therefore suggest relatively high rates of mutation, as expected, given the intrinsically errorprone nature of RNA replication (15, 65). As well as the difference...

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confidence: 99%

Long-Term Evolution of theLuteoviridae: Time Scale and Mode of Virus Speciation

Pagán

Holmes

2010

J Virol

126

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“…RNA viruses have a high mutation rate that increases their genetic diversity over time (Belshaw et al, 2007;Domingo et al, 2012;Lemey et al, 2006) and the segmented nature of the IAV genome allows the virus to exchange (reassort) gene segments with other IAVs, thus contributing to the overall genetic diversity of IAVs.…”

Section: Introductionmentioning

confidence: 99%

Genome plasticity of triple-reassortant H1N1 influenza A virus during infection of vaccinated pigs

Díaz

Enomoto

Romagosa

et al. 2015

Journal of General Virology

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To gain insight into the evolution of influenza A viruses (IAVs) during infection of vaccinated pigs, we experimentally infected a 3-week-old naive pig with a triple-reassortant H1N1 IAV and placed the seeder pig in direct contact with a group of age-matched vaccinated pigs (n510). We indexed the genetic diversity and evolution of the virus at an intra-host level by deep sequencing the entire genome directly from nasal swabs collected at two separate samplings during infection. We obtained 13 IAV metagenomes from 13 samples, which included the virus inoculum and two samples from each of the six pigs that tested positive for IAV during the study. The infection produced a population of heterogeneous alleles (sequence variants) that was dynamic over time. Overall, 794 polymorphisms were identified amongst all samples, which yielded 327 alleles, 214 of which were unique sequences. A total of 43 distinct haemagglutinin proteins were translated, two of which were observed in multiple pigs, whereas the neuraminidase (NA) was conserved and only one dominant NA was found throughout the study. The genetic diversity of IAVs changed dynamically within and between pigs. However, most of the substitutions observed in the internal gene segments were synonymous. Our results demonstrated remarkable IAV diversity, and the complex, rapid and dynamic evolution of IAV during infection of vaccinated pigs that can only be appreciated with repeated sampling of individual animals and deep sequence analysis.

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“…In stark contrast, gene order within virus orders and families is often conserved. Viral genomes tend to be smaller, with minimal intergenic sequences and in some cases overlapping genes (Lynch 2006;Belshaw et al 2007;Koonin 2009). The reasons why a particular gene order supports the required patterns of virus gene expression and virus replication have in many cases also been elucidated.…”

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Multiple Barriers to the Evolution of Alternative Gene Orders in a Positive-Strand RNA Virus

et al. 2016

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The order in which genes are organized within a genome is generally not conserved between distantly related species. However, within virus orders and families, strong conservation of gene order is observed. The factors that constrain or promote gene-order diversity are largely unknown, although the regulation of gene expression is one important constraint for viruses. Here we investigate why gene order is conserved for a positive-strand RNA virus encoding a single polyprotein in the context of its authentic multicellular host. Initially, we identified the most plausible trajectory by which alternative gene orders could evolve. Subsequently, we studied the accessibility of key steps along this evolutionary trajectory by constructing two virus intermediates: (1) duplication of a gene followed by (2) loss of the ancestral gene. We identified five barriers to the evolution of alternative gene orders. First, the number of viable positions for reordering is limited. Second, the within-host fitness of viruses with gene duplications is low compared to the wild-type virus. Third, after duplication, the ancestral gene copy is always maintained and never the duplicated one. Fourth, viruses with an alternative gene order have even lower fitness than viruses with gene duplications. Fifth, after more than half a year of evolution in isolation, viruses with an alternative gene order are still vastly inferior to the wild-type virus. Our results show that all steps along plausible evolutionary trajectories to alternative gene orders are highly unlikely. Hence, the inaccessibility of these trajectories probably contributes to the conservation of gene order in present-day viruses.

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The evolution of genome compression and genomic novelty in RNA viruses

Cited by 150 publications

References 47 publications

Long-Term Evolution of theLuteoviridae: Time Scale and Mode of Virus Speciation

Long-Term Evolution of theLuteoviridae: Time Scale and Mode of Virus Speciation

Genome plasticity of triple-reassortant H1N1 influenza A virus during infection of vaccinated pigs

Multiple Barriers to the Evolution of Alternative Gene Orders in a Positive-Strand RNA Virus

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