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

Adérito L Monjane,Gordon W Harkins,Natasha Wood,Guy Triton,Betty E Owor,Wayne Delport,Salem Saumtally,Dionne N Shepherd,Edward P Rybicki,Lara Donaldson,Rob W Briddon,Darren P Martin,Siobain Duffy,Arvind Varsani

doi:10.1186/1743-422x-6-104

Abstract

BackgroundDespite 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.ResultsWe have conducted long-term evolution experiments lasting between 6 and 32 years, where we have determined substitution rates of between 2 and 3 × 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.ConclusionThe 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.

Highlights

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 codiverged with their hosts over millions of years
The best supported, non-exclusive theories that have so far been put forward to explain discrepancies between basal mutation rates of single-stranded DNA (ssDNA) viruses and their hosts are that: (1) when in a ssDNA state the genomes of these viruses are subject to mutagenic processes that are less frequently experienced in dsDNA [4]; (2) geminivirus genomes, and those of some other ssDNA viruses, are not sufficiently methylated such that normal host mechanisms of mismatch repair may not function during their replication [16,17]; and (3) when replicating, ssDNA virus genomes are only transiently double stranded such that when errors occur they are not efficiently repaired by host base-excision pathways [4]
Our results provide extensive additional support for the hypothesis that, as with other geminiviruses, Maize streak virus (MSV) and Sugarcane streak Réunion virus (SSRV) basal mutation rates are possibly elevated by unrepaired oxidative damage inflicted on ssDNA

Summary

Introduction

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 codiverged 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. While the inherent infidelities of RNA polymerases and reverse transcriptases drive the high rates of evolution seen in RNA viruses, all known ssDNA viruses replicate using presumably high-fidelity host DNA polymerases. Adopting the convention of Duffy et al [15] we differentiate between the biochemical or basal rate at which mutations arise (mutation rate, measured in rounds of genomic replication or units of time), and the usually slower rate at which mutations accumulate in wild populations evolving under natural selection (substitution rate, usually measured in years)

Methods

Results

Conclusion