Abstract
Viral recombination can dramatically impact evolution and epidemiology. In viruses, the recombination rate depends on the frequency of genetic exchange between different viral genomes within an infected host cell and on the frequency at which such co-infections occur. While the recombination rate has been recently evaluated in experimentally co-infected cell cultures for several viruses, direct quantification at the most biologically significant level, that of a host infection, is still lacking. This study fills this gap using the cauliflower mosaic virus as a model. We distributed four neutral markers along the viral genome, and co-inoculated host plants with marker-containing and wild-type viruses. The frequency of recombinant genomes was evaluated 21 d post-inoculation. On average, over 50% of viral genomes recovered after a single host infection were recombinants, clearly indicating that recombination is very frequent in this virus. Estimates of the recombination rate show that all regions of the genome are equally affected by this process. Assuming that ten viral replication cycles occurred during our experiment—based on data on the timing of coat protein detection—the per base and replication cycle recombination rate was on the order of 2 × 10−5 to 4 × 10−5. This first determination of a virus recombination rate during a single multi-cellular host infection indicates that recombination is very frequent in the everyday life of this virus.
Highlights
As increasing numbers of full-length viral sequences become available, recombinant or mosaic viruses are being recognized more frequently [1,2,3]
Progeny can become hybrid through different mechanisms, such as reassortment of segments when the parental genomes are fragmented [10], intra-molecular recombination when polymerases switch templates [11], or homologous or non-homologous recombination
The proportion of recombinant genomes found in the mixed viral populations was astonishingly high and very similar in the ten co-infected plants analyzed (Table 1, last column), ranging between 44% to 60%, with a mean frequency (6 standard error) of 53.8% 6 2.0%. This result indicates that recombination events are very frequent during the invasion of the host plant by cauliflower mosaic virus (CaMV) and represents, to our knowledge, the first direct quantification of viral recombination during the infection of a live multi-cellular host
Summary
As increasing numbers of full-length viral sequences become available, recombinant or mosaic viruses are being recognized more frequently [1,2,3]. The in vitro approach, which has so far been applied only to animal viruses, allows the establishment of the ‘‘intrinsic’’ recombination rate in experimentally co-infected cells in cell cultures [14,15,19]. It does not necessarily reflect the situation in entire, living hosts, where the frequency of coinfected cells is poorly known and depends on many factors such as the size of the pathogen population, the relative frequency and distribution of the different variants, and host defense mechanisms preventing secondary infection of cells. The in vivo experimental approach is closer to biological conditions and may be more informative of what happens in ‘‘the real world.’’
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