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

ArticleinJournal of General Virology 90(Pt 6):1539-47 · April 2009with16 Reads
DOI: 10.1099/vir.0.009266-0 · Source: PubMed
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 (1997-2002) 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 1.60x10(-3) and 1.33x10(-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.
    • "A negative or zero correlation coefficient would imply that the data are absolutely not clocklike and then that the genetic variability evident in the data could not be properly related to sampling times (i.e., the absence of sufficient temporal signal in the dataset to confidently infer coalescence times or substitution rates). Secondly, we performed a tip-date randomization technique previously described in other studies [29, 62] . For each dataset, ten independent randomizations of the sampling dates associated with each sequence were performed. "
    [Show abstract] [Hide abstract] ABSTRACT: Background Cassava mosaic disease (CMD) in Madagascar is caused by a complex of at least six African cassava mosaic geminivirus (CMG) species. This provides a rare opportunity for a comparative study of the evolutionary and epidemiological dynamics of distinct pathogenic crop-infecting viral species that coexist within the same environment. The genetic and spatial structure of CMG populations in Madagascar was studied and Bayesian phylogeographic modelling was applied to infer the origins of Madagascan CMG populations within the epidemiological context of related populations situated on mainland Africa and other south western Indian Ocean (SWIO) islands. ResultsThe isolation and analysis of 279 DNA-A and 117 DNA-B sequences revealed the presence in Madagascar of four prevalent CMG species (South African cassava mosaic virus, SACMV; African cassava mosaic virus, ACMV; East African cassava mosaic Kenya virus, EACMKV; and East African cassava mosaic Cameroon virus, EACMCV), and of numerous CMG recombinants that have, to date, only ever been detected on this island. SACMV and ACMV, the two most prevalent viruses, displayed low degrees of genetic diversity and have most likely been introduced to the island only once. By contrast, EACMV-like CMG populations (consisting of East African cassava mosaic virus, EAMCKV, EACMCV and complex recombinants of these) were more diverse, more spatially structured, and displayed evidence of at least three independent introductions from mainland Africa. Although there were no statistically supported virus movement events between Madagascar and the other SWIO islands, at least one mainland African ACMV variant likely originated in Madagascar. Conclusions Our study highlights both the complexity of CMD in Madagascar, and the distinct evolutionary and spatial dynamics of the different viral species that collectively are associated with this disease. Given that more distinct CMG species and recombinants have been found in Madagascar than any other similarly sized region of the world, the risks of recombinant CMG variants emerging on this island are likely to be higher than elsewhere. Evidence of an epidemiological link between Madagascan and mainland African CMGs suggests that the consequences of such emergence events could reach far beyond the shores of this island.
    Full-text · Article · Dec 2016
    • "Black triangles highlight events with particular biological significance as discussed in the text. der Walt et al., 2008; Duffy and Holmes, 2009). Frequencies of single-nucleotide insertions (ins) and deletions (del) of viral components (Fig. 5C and D) appear higher, but these differences are less informative as they come mostly from single loci with poly G stretches (nucleotide positions 1458-GGGGGG-1463 for insertions in DNA A; 2476-GGGGG-2480 for deletions in DNA B). "
    [Show abstract] [Hide abstract] ABSTRACT: To study a possible role for homologous recombination in geminivirus replication, we challenged Arabidopsis recombination gene knockouts by Euphorbia yellow mosaic virus infection. Our results show that the RAD51 paralog RAD51D, rather than RAD51 itself, promotes viral replication at early stages of infection. Blot hybridization analyses of replicative intermediates using one- and two-dimensional gels and deep sequencing point to an unexpected facet of recombination-dependent replication, the repair by single-strand annealing (SSA) during complementary strand replication. A significant decrease of both intramolecular, yielding defective DNAs and intermolecular recombinant molecules between the two geminiviral DNA components (A, B) were observed in the absence of RAD51D. By contrast, DNA A and B reacted differentially with the generation of inversions. A model to implicate single-strand annealing recombination in geminiviral recombination-dependent replication is proposed.
    Article · Jun 2016
    • "Similarly, BYVMV has also been found in many countries, including Pakistan , India, Bangladesh and Thailand [12,35,36]. Our analysis revealed that CGs have high substitution rates, just like other known geminiviruses infecting tomatoes and cassava [18,19] . Since fewer sequences were available for CLCu- KoV, we chose the CP gene of Burewala as the dataset for CLCuKoV. "
    [Show abstract] [Hide abstract] ABSTRACT: The spread of cotton leaf curl disease in China, India and Pakistan is a recent phenomenon. Analysis of available sequence data determined that there is a substantial diversity of cotton-infecting geminiviruses in Pakistan. Phylogenetic analyses indicated that recombination between two major groups of viruses, cotton leaf curl Multan virus (CLCuMuV) and cotton leaf curl Kokhran virus (CLCuKoV), led to the emergence of several new viruses. Recombination detection programs and phylogenetic analyses showed that CLCuMuV and CLCuKoV are highly recombinant viruses. Indeed, CLCuKoV appeared to be a major donor virus for the coat protein (CP) gene, while CLCuMuV donated the Rep gene in the majority of recombination events. Using recombination free nucleotide datasets the substitution rates for CP and Rep genes were determined. We inferred similar nucleotide substitution rates for the CLCuMuV-Rep gene (4.96X10-4) and CLCuKoV-CP gene (2.706X10-4), whereas relatively higher substitution rates were observed for CLCuMuV-CP and CLCuKoV-Rep genes. The combination of sequences with equal and relatively low substitution rates, seemed to result in the emergence of viral isolates that caused epidemics in Pakistan and India. Our findings also suggest that CLCuMuV is spreading at an alarming rate, which can potentially be a threat to cotton production in the Indian subcontinent.
    Full-text · Article · Mar 2016
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