Rapid evolutionary dynamics of zucchini yellow mosaic virus

Simmons, H. E.; Holmes, Edward C.; Stephenson, Andrew G.

doi:10.1099/vir.0.83543-0

Cited by 55 publications

(32 citation statements)

References 35 publications

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“…Analysis of the full-length genomic DNA sequences revealed that the level of genetic variation observed in the natural population of TYLCV (1.69×10 -3 subs/site/year) was similar to that found in RNA viruses Simmons et al, 2008;. These and other results suggest that a considerable amount of sequence variation occurs within and between populations of geminiviruses, challenging the view that RNA viruses are prone to higher mutation rates than DNA viruses (Domingo and Holland, 1997;Roossinck, 1997;Isnard et al, 1998;Sanz et al, 1999).…”

Section: Discussionmentioning

confidence: 79%

Molecular variability and evolution of a natural population of tomato yellow leaf curl virus in Shanghai, China

Yang

Zhou

Qian

et al. 2014

J. Zhejiang Univ. Sci. B

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Tomato yellow leaf curl virus (TYLCV), belonging to the genus Begomovirus of the family Geminiviridae, is emerging as the most destructive pathogen of tomato plants. Since the first report of TYLCV in Shanghai, China in 2006, TYLCV has spread rapidly to 13 provinces or autonomous regions of China. In this study, the molecular variability and evolution of TYLCV were monitored in Shanghai from its first upsurge in 2006 until 2010. Full-length genomic sequences of 26 isolates were obtained by rolling circle amplification. Sequence analysis showed that the intergenic region was the most variable, with a mean mutation rate of 4.81×10 −3 nucleotide substitutions per site per year. Genetic differentiation was found within isolates obtained from 2006, 2009, and 2010, though a linear increase in genetic diversity over time was not evident. Whilst significant parts of TYLCV genes were under negative selection, the C4 gene embedded entirely within the C1 gene had a tendency to undergo positive selection. Our results indicate that a mechanism of independent evolution of overlapping regions could apply to the natural population of TYLCV in Shanghai, China.

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Section: Discussionmentioning

confidence: 79%

Molecular variability and evolution of a natural population of tomato yellow leaf curl virus in Shanghai, China

Yang

Zhou

Qian

et al. 2014

J. Zhejiang Univ. Sci. B

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“…Finally, we observed that all individual luteovirus species appeared within the last 500 years. It is striking that the dates estimated for the majority of these speciation events fall into the same range as those of the Potyviridae and of other families of plant RNA viruses (17,24,43,69). Given this overall similarity in evolutionary patterns, we hypothesize that the intensification of agriculture in the modern era, which resulted in an increase in cultivated plant populations, as well as the establishment of global communication networks, had a major effect on the extent and structure of genetic variation in multiple plant RNA viruses.…”

Section: Discussionmentioning

confidence: 87%

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

Pagán

Holmes

2010

J Virol

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128

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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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“…For instance, while many rigorous estimates of rates of nucleotide substitution exist for mammalian RNA viruses (e.g. Chen & Holmes, 2006;Hanada et al, 2004;Jenkins et al, 2002;Ramsden et al, 2008), only in the past year have well-supported estimates of substitution rates of plant viruses been published: for the positive-sense singlestranded RNA (ssRNA+) viruses rice yellow mottle virus (Fargette et al, 2008), zucchini yellow mosaic virus (Simmons et al, 2008), a broad group of potyviruses (Gibbs et al, 2008), and the single-stranded DNA (ssDNA) tomato yellow leaf curl virus (TYLCV; . Importantly, these data challenge earlier ideas that plant viruses evolve more slowly than animal viruses (Blok et al, 1987;Fraile et al, 1997) (Jenkins et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses

Duffy

Holmes

2009

Journal of General Virology

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173

140

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Whitefly-transmitted geminiviruses are major pathogens of the important crop cassava in Africa. The intensive sampling and sequencing of cassava mosaic disease-causing viruses that occurred in the wake of a severe outbreak in Central Africa (1997)(1998)(1999)(2000)(2001)(2002) allowed us to estimate the rate of evolution of this virus. East African cassava mosaic virus and related species are obligately bipartite (DNA-A and DNA-B segments), and these two genome segments have different evolutionary histories. Despite these phylogenetic differences, we inferred high rates of nucleotide substitution in both segments: mean rates of 1.60¾10"3 and 1.33¾10 "4 substitutions site "1 year "1 for DNA-A and DNA-B, respectively. While similarly high substitution rates were found in datasets free of detectable recombination, only that estimated for the coat protein gene (AV1), for which an additional DNA-A sequence isolated in 1995 was available, was statistically robust. These high substitution rates also confirm that those previously estimated for the monopartite tomato yellow leaf curl virus (TYLCV) are representative of multiple begomoviruses. We also validated our rate estimates by comparing them with those depicting the emergence of TYLCV in North America. These results further support the notion that geminiviruses evolve as rapidly as many RNA viruses.

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Rapid evolutionary dynamics of zucchini yellow mosaic virus

Cited by 55 publications

References 35 publications

Molecular variability and evolution of a natural population of tomato yellow leaf curl virus in Shanghai, China

Molecular variability and evolution of a natural population of tomato yellow leaf curl virus in Shanghai, China

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

Validation of high rates of nucleotide substitution in geminiviruses: phylogenetic evidence from East African cassava mosaic viruses

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