Abstract

BackgroundRecent reports have indicated that single-stranded DNA (ssDNA) viruses in the taxonomic families Geminiviridae, Parvoviridae and Anellovirus may be evolving at rates of ~10-4 substitutions per site per year (subs/site/year). These evolution rates are similar to those of RNA viruses and are surprisingly high given that ssDNA virus replication involves host DNA polymerases with fidelities approximately 10 000 times greater than those of error-prone viral RNA polymerases. Although high ssDNA virus evolution rates were first suggested in evolution experiments involving the geminivirus maize streak virus (MSV), the evolution rate of this virus has never been accurately measured. Also, questions regarding both the mechanistic basis and adaptive value of high geminivirus mutation rates remain unanswered.ResultsWe determined the short-term evolution rate of MSV using full genome analysis of virus populations initiated from cloned genomes. Three wild type viruses and three defective artificial chimaeric viruses were maintained in planta for up to five years and displayed evolution rates of between 7.4 × 10-4 and 7.9 × 10-4 subs/site/year.ConclusionThese MSV evolution rates are within the ranges observed for other ssDNA viruses and RNA viruses. Although no obvious evidence of positive selection was detected, the uneven distribution of mutations within the defective virus genomes suggests that some of the changes may have been adaptive. We also observed inter-strand nucleotide substitution imbalances that are consistent with a recent proposal that high mutation rates in geminiviruses (and possibly ssDNA viruses in general) may be due to mutagenic processes acting specifically on ssDNA molecules.

Highlights

  • Recent reports have indicated that single-stranded DNA viruses in the taxonomic families Geminiviridae, Parvoviridae and Anellovirus may be evolving at rates of ~10-4 substitutions per site per year

  • In addition to estimating the short-term maize streak virus (MSV) evolution rate within individual hosts, we present evidence that MSV exhibits strand specific nucleotide substitution imbalances that are consistent with a recent proposal by Duffy and Holmes [30] that high mutation rates in single-stranded DNA (ssDNA) viruses are due to mutagenic processes that affect ssDNA molecules

  • Mutations occur at high frequencies during MSV infections With the intention of studying evolution rates and patterns of nucleotide substitution in MSV, sweetcorn plants were initially agroinoculated with clones of three wildtype MSV strains – MSV-Tas, MSV-Kom and MSV-Set – and three defective laboratory constructed recombinant viruses – K-MP-S, K-MP-CP-S and S-CP-K (Figure 1)

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Summary

Introduction

Recent reports have indicated that single-stranded DNA (ssDNA) viruses in the taxonomic families Geminiviridae, Parvoviridae and Anellovirus may be evolving at rates of ~10-4 substitutions per site per year (subs/site/year). These evolution rates are similar to those of RNA viruses and are surprisingly high given that ssDNA virus replication involves host DNA polymerases with fidelities approximately 10 000 times greater than those of error-prone viral RNA polymerases. And possibly contradicting the premise that polymerase fidelity is the major universal determinant of evolution rates, figures closer to those of RNA viruses (~10-4 subs/site/year) have been reported for the small single stranded DNA (ssDNA) anelloviruses [7,8,9] and parvoviruses [10,11,12]. Interest in geminivirus evolution has, until recently, been largely focussed on the undeniably important role of recombination in the generation of novel species and strains [20,21,22,23,24,25], it is the accumulation of point mutations that is the ultimate source of diversity within the family

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