Experimental Evolution of Pseudogenization and Gene Loss in a Plant RNA Virus

Zwart, Mark P.; Willemsen, Anouk; Daròs, José‐Antonio; Elena, Santiago F.

doi:10.1093/molbev/mst175

Cited by 42 publications

(102 citation statements)

References 62 publications

(100 reference statements)

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“…Because the deletion occurs at the start of the genome, it is not necessary to maintain the reading frame as long as the original second methionine in P1 is preserved. In TEV-NIb 2 -NIb 9 , none of the deletions included the C-terminus of P1, but for seven of ten lineages the deletions included the N-terminal region of the HC-Pro cysteine protease (Figure 6), similar to results obtained by previous studies Zwart et al 2014). HC-Pro cysteine protease is a multifunctional protein, and the N-terminal region of HC-Pro cysteine protease is implicated in transmission by aphids (Thornbury et al 1990;Atreya et al 1992) and is not essential for replication and movement Cronin et al 1995).…”

Section: Whole-genome Sequences Of Evolved Lineages Of Viruses With Asupporting

confidence: 86%

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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Section: Whole-genome Sequences Of Evolved Lineages Of Viruses With Asupporting

confidence: 86%

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

et al. 2016

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“…Third, in both hosts we observe only one evolved lineage with increases in within-host competitive fitness, and surprisingly the eGFP marker does not seem to have a fitness cost in N. benthamiana. These results were unexpected based on our previous work in N. tabacum [21], but they do exemplify the extent to which a host species jump can be a game changer for RNA virus evolutionary dynamics.…”

Section: Introductioncontrasting

confidence: 60%

“…Experimental setup and fluorescent marker stability upon passaging of TEV-eGFP TEV-eGFP was mechanically passaged in N. benthamiana and D. stramonium, as described in Zwart et al 2014 [21]. In this previous study, we noted that 9-week long passages led to rapid deletion of eGFP as well as rapid convergent evolution in N. tabacum [21].…”

Section: Resultsmentioning

confidence: 99%

“…This exogenous sequence of 762 nts increases TEV genome to a size just over 10 kb. Upon longduration passages in N. tabacum, the eGFP gene is quickly lost due to its strong fitness cost, and its loss is reliably indicated by a loss of eGFP fluorescence [21]. Therefore, we can use the time to eGFP loss in the virus population as a real-time indicator of adaptation.…”

Section: Introductionmentioning

confidence: 99%

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High virulence does not necessarily impede viral adaptation to a new host: A case study using a plant RNA virus

Willemsen

Zwart

Elena

2016

Preprint

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Background: Theory suggests that high virulence could hinder between-host transmission of microparasites, and that virulence therefore will evolve to lower levels. Alternatively, highly virulent microparasites could also curtail host development, thereby limiting both the host resources available to them and their own within-host effective population size. In this case, high virulence might restrain the mutation supply rate and increase the strength with which genetic drift acts on microparasite populations. Thereby, this alternative explanation limits the microparasites' potential to adapt to the host and ultimately the ability to evolve lower virulence. As a first exploration of this hypothesis, we evolved Tobacco etch virus carrying an eGFP fluorescent marker in two semi-permissive host species, Nicotiana benthamiana and Datura stramonium, for which it has a large difference in virulence. We compared the results to those previously obtained in the natural host, Nicotiana tabacum, where we have shown that carriage of eGFP has a high fitness cost and its loss serves as a real-time indicator of adaptation.Results: After over half a year of evolution, we sequenced the genomes of the evolved lineages and measured their fitness. During the evolution experiment, marker loss leading to viable virus variants was only observed in one lineage of the host for which the virus has low virulence, D. stramonium. This result was consistent with the observation that there was a fitness cost of eGFP in this host, while surprisingly no fitness cost was observed in the host for which the virus has high virulence, N. benthamiana. Furthermore, in both hosts we observed increases in viral fitness in few lineages, and host-specific convergent evolution at the genomic level was only found in N. benthamiana. Conclusions:The results of this study do not lend support to the hypothesis that high virulence impedes microparasites' evolution. Rather, they exemplify that jumps between host species can be game changers for evolutionary dynamics. When considering the evolution of genome architecture, host species jumps might play a very important role, by allowing evolutionary intermediates to be competitive.

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“…In the first of a series of recent experiments, Zwart et al [15] explored the dynamics of gene acquisition and loss. In an initial study, a genome carrying an additional gene inframe with TEV single open reading frame was generated (figure 2a).…”

Section: Flexible Rna Genomes: Gene Gains and Lossesmentioning

confidence: 99%

Evolutionary transitions during RNA virus experimental evolution

Elena

2016

Phil. Trans. R. Soc. B

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One contribution of 13 to a theme issue 'The major synthetic evolutionary transitions'. In their search to understand the evolution of biological complexity, John Maynard Smith and Eörs Szathmáry put forward the notion of major evolutionary transitions as those in which elementary units get together to generate something new, larger and more complex. The origins of chromosomes, eukaryotic cells, multicellular organisms, colonies and, more recently, language and technological societies are examples that clearly illustrate this notion. However, a transition may be considered as anecdotal or as major depending on the specific level of biological organization under study. In this contribution, I will argue that transitions may also be occurring at a much smaller scale of biological organization: the viral world. Not only that, but also that we can observe in real time how these major transitions take place during experimental evolution. I will review the outcome of recent evolution experiments with viruses that illustrate four major evolutionary transitions: (i) the origin of a new virus that infects an otherwise inaccessible host and completely changes the way it interacts with the host regulatory and metabolic networks, (ii) the incorporation and loss of genes, (iii) the origin of segmented genomes from a non-segmented one, and (iv) the evolution of cooperative behaviour and cheating between different viruses or strains during co-infection of the same host.This article is part of the themed issue 'The major synthetic evolutionary transitions'.

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Experimental Evolution of Pseudogenization and Gene Loss in a Plant RNA Virus

Cited by 42 publications

References 62 publications

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

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

High virulence does not necessarily impede viral adaptation to a new host: A case study using a plant RNA virus

Evolutionary transitions during RNA virus experimental evolution

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