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Experimental evidence indicating that mastreviruses probably did not co-diverge with their hosts.

Harkins GW, Delport W, Duffy S, Wood N, Monjane AL, Owor BE, Donaldson L, Saumtally S, Triton G, Briddon RW, Shepherd DN, Rybicki EP, Martin DP, Varsani A - Virol. J. (2009)

Bottom Line: This "co-divergence hypothesis" requires that long-term mastrevirus substitution rates be at least 100,000-fold lower than their basal mutation rates and 10,000-fold lower than their observable short-term substitution rates.We further show that mutation biases are similar for different geminivirus genera, suggesting that mutational processes that drive high basal mutation rates are conserved across the family.The absence of strong negative selection signals within our evolution experiments and the uniformly high geminivirus substitution rates that we and others have reported suggest that mastreviruses cannot have co-diverged with their hosts.

View Article: PubMed Central - HTML - PubMed

Affiliation: South African National Bioinformatics Institute, University of the Western Cape, Cape Town, South Africa. gordon@sanbi.ac.za

ABSTRACT

Background: Despite the demonstration that geminiviruses, like many other single stranded DNA viruses, are evolving at rates similar to those of RNA viruses, a recent study has suggested that grass-infecting species in the genus Mastrevirus may have co-diverged with their hosts over millions of years. This "co-divergence hypothesis" requires that long-term mastrevirus substitution rates be at least 100,000-fold lower than their basal mutation rates and 10,000-fold lower than their observable short-term substitution rates. The credibility of this hypothesis, therefore, hinges on the testable claim that negative selection during mastrevirus evolution is so potent that it effectively purges 99.999% of all mutations that occur.

Results: We have conducted long-term evolution experiments lasting between 6 and 32 years, where we have determined substitution rates of between 2 and 3 x 10(-4) substitutions/site/year for the mastreviruses Maize streak virus (MSV) and Sugarcane streak Réunion virus (SSRV). We further show that mutation biases are similar for different geminivirus genera, suggesting that mutational processes that drive high basal mutation rates are conserved across the family. Rather than displaying signs of extremely severe negative selection as implied by the co-divergence hypothesis, our evolution experiments indicate that MSV and SSRV are predominantly evolving under neutral genetic drift.

Conclusion: The absence of strong negative selection signals within our evolution experiments and the uniformly high geminivirus substitution rates that we and others have reported suggest that mastreviruses cannot have co-diverged with their hosts.

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Description of datasets. (a) Phylogenetic comparison of sequences from experimental evolution experiments (left) and sequences sampled from nature (right), all drawn to the same scale. Whereas the SSRV-A (32 years), MSV-F (6 years) and MSV-B (6 years) datasets are described here for the first time, the MSV-B (5 years), MSV-A, and WDV datasets are those described by van der Walt et al. [9], Varsani et al. [26] and Ramsel et al. [28], respectively. Black dots indicate likely rooting positions as determined by an outgroup. Best fit models used during maximum likelihood tree construction are GTR+I+Γ4 for the SSRV, WDV and MSV-A trees, F81+Γ4 for the MSV-B five-year and MSV-F six-year trees and TN93+Γ4 for the MSV-B six-year tree. (b) Evolution experiment datasets indicating the sources and timing of sequence sampling.
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Figure 1: Description of datasets. (a) Phylogenetic comparison of sequences from experimental evolution experiments (left) and sequences sampled from nature (right), all drawn to the same scale. Whereas the SSRV-A (32 years), MSV-F (6 years) and MSV-B (6 years) datasets are described here for the first time, the MSV-B (5 years), MSV-A, and WDV datasets are those described by van der Walt et al. [9], Varsani et al. [26] and Ramsel et al. [28], respectively. Black dots indicate likely rooting positions as determined by an outgroup. Best fit models used during maximum likelihood tree construction are GTR+I+Γ4 for the SSRV, WDV and MSV-A trees, F81+Γ4 for the MSV-B five-year and MSV-F six-year trees and TN93+Γ4 for the MSV-B six-year tree. (b) Evolution experiment datasets indicating the sources and timing of sequence sampling.

Mentions: To assess sequence divergence over time in these three serendipitous evolution experiments, we cloned and sequenced between 8 and 20 complete viral genomes from each of the six SSRV samples (a total of 81 clones), the two MSV-B samples (a total of 18 clones) and the two MSV-F samples (a total of 22 clones; see Table 1 for a breakdown of samples from which clones were obtained). We found that the viral diversity within the various experimental plants over the duration of the experiment was surprisingly high when compared with that observed within natural continent-wide MSV and WDV populations (Figure 1a). For example, the degree of virus diversification noted over the 32-year SSRV experiment is approximately (1) half that found for the major southern African MSV-A variant [26], MSV-A4, and (2) equivalent to that found throughout China for the wheat-adapted WDV strain [28].


Experimental evidence indicating that mastreviruses probably did not co-diverge with their hosts.

Harkins GW, Delport W, Duffy S, Wood N, Monjane AL, Owor BE, Donaldson L, Saumtally S, Triton G, Briddon RW, Shepherd DN, Rybicki EP, Martin DP, Varsani A - Virol. J. (2009)

Description of datasets. (a) Phylogenetic comparison of sequences from experimental evolution experiments (left) and sequences sampled from nature (right), all drawn to the same scale. Whereas the SSRV-A (32 years), MSV-F (6 years) and MSV-B (6 years) datasets are described here for the first time, the MSV-B (5 years), MSV-A, and WDV datasets are those described by van der Walt et al. [9], Varsani et al. [26] and Ramsel et al. [28], respectively. Black dots indicate likely rooting positions as determined by an outgroup. Best fit models used during maximum likelihood tree construction are GTR+I+Γ4 for the SSRV, WDV and MSV-A trees, F81+Γ4 for the MSV-B five-year and MSV-F six-year trees and TN93+Γ4 for the MSV-B six-year tree. (b) Evolution experiment datasets indicating the sources and timing of sequence sampling.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2719613&req=5

Figure 1: Description of datasets. (a) Phylogenetic comparison of sequences from experimental evolution experiments (left) and sequences sampled from nature (right), all drawn to the same scale. Whereas the SSRV-A (32 years), MSV-F (6 years) and MSV-B (6 years) datasets are described here for the first time, the MSV-B (5 years), MSV-A, and WDV datasets are those described by van der Walt et al. [9], Varsani et al. [26] and Ramsel et al. [28], respectively. Black dots indicate likely rooting positions as determined by an outgroup. Best fit models used during maximum likelihood tree construction are GTR+I+Γ4 for the SSRV, WDV and MSV-A trees, F81+Γ4 for the MSV-B five-year and MSV-F six-year trees and TN93+Γ4 for the MSV-B six-year tree. (b) Evolution experiment datasets indicating the sources and timing of sequence sampling.
Mentions: To assess sequence divergence over time in these three serendipitous evolution experiments, we cloned and sequenced between 8 and 20 complete viral genomes from each of the six SSRV samples (a total of 81 clones), the two MSV-B samples (a total of 18 clones) and the two MSV-F samples (a total of 22 clones; see Table 1 for a breakdown of samples from which clones were obtained). We found that the viral diversity within the various experimental plants over the duration of the experiment was surprisingly high when compared with that observed within natural continent-wide MSV and WDV populations (Figure 1a). For example, the degree of virus diversification noted over the 32-year SSRV experiment is approximately (1) half that found for the major southern African MSV-A variant [26], MSV-A4, and (2) equivalent to that found throughout China for the wheat-adapted WDV strain [28].

Bottom Line: This "co-divergence hypothesis" requires that long-term mastrevirus substitution rates be at least 100,000-fold lower than their basal mutation rates and 10,000-fold lower than their observable short-term substitution rates.We further show that mutation biases are similar for different geminivirus genera, suggesting that mutational processes that drive high basal mutation rates are conserved across the family.The absence of strong negative selection signals within our evolution experiments and the uniformly high geminivirus substitution rates that we and others have reported suggest that mastreviruses cannot have co-diverged with their hosts.

View Article: PubMed Central - HTML - PubMed

Affiliation: South African National Bioinformatics Institute, University of the Western Cape, Cape Town, South Africa. gordon@sanbi.ac.za

ABSTRACT

Background: Despite the demonstration that geminiviruses, like many other single stranded DNA viruses, are evolving at rates similar to those of RNA viruses, a recent study has suggested that grass-infecting species in the genus Mastrevirus may have co-diverged with their hosts over millions of years. This "co-divergence hypothesis" requires that long-term mastrevirus substitution rates be at least 100,000-fold lower than their basal mutation rates and 10,000-fold lower than their observable short-term substitution rates. The credibility of this hypothesis, therefore, hinges on the testable claim that negative selection during mastrevirus evolution is so potent that it effectively purges 99.999% of all mutations that occur.

Results: We have conducted long-term evolution experiments lasting between 6 and 32 years, where we have determined substitution rates of between 2 and 3 x 10(-4) substitutions/site/year for the mastreviruses Maize streak virus (MSV) and Sugarcane streak Réunion virus (SSRV). We further show that mutation biases are similar for different geminivirus genera, suggesting that mutational processes that drive high basal mutation rates are conserved across the family. Rather than displaying signs of extremely severe negative selection as implied by the co-divergence hypothesis, our evolution experiments indicate that MSV and SSRV are predominantly evolving under neutral genetic drift.

Conclusion: The absence of strong negative selection signals within our evolution experiments and the uniformly high geminivirus substitution rates that we and others have reported suggest that mastreviruses cannot have co-diverged with their hosts.

Show MeSH
Related in: MedlinePlus