The Evolutionary Value of Recombination Is Constrained by Genome Modularity

Institute of Infectious Diseases and Molecular Medicine, University of Cape Town, Cape Town, South Africa.
PLoS Genetics (Impact Factor: 8.17). 11/2005; 1(4):e51. DOI: 10.1371/journal.pgen.0010051
Source: PubMed


Genetic exchange between organisms, called recombination, occurs in all biological kingdoms and is also common in viruses in which it may threaten the long-term control of important human pathogens such as HIV and influenza. Although recombination can produce advantageous gene combinations, bioinformatic analyses of bacterial genomes have suggested that recombination is not well tolerated when it involves exchanges of genes that interact with a lot of other genes. Using laboratory-constructed recombinants of a small plant virus called MSV, Martin and co-workers provide the first direct experimental evidence that the evolutionary value of exchanging a genome fragment is constrained by the number of ways in which the fragment interacts with the rest of the genome. They note that fitness losses suffered by artificial MSV recombinants increase with decreasing parental relatedness. Furthermore, these losses accurately anticipate the patterns of genetic exchange detectable in natural MSV recombinants, suggesting that they accurately reflect the impact of deleterious selection on natural isolates of the virus.

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Available from: Ed Rybicki, Aug 14, 2015
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    • "Similar results were observed for tomato-infecting begomoviruses in Brazil, which are thought to have arisen from inter-species recombination between begomoviruses infecting non-cultivated hosts (Ribeiro et al., 2007; Rocha et al., 2013). Although some studies indicate that a large number of recombinants arising from events between distantly related genomes are defective and probably would be removed from the population by selection (Liu et al., 1999; Martin et al., 2005), our results continue to emphasize the importance of recombination for microevolution and macroevolution of agronomically important begomo- viruses. "
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    ABSTRACT: Begomoviruses are whitefly-transmitted, single-stranded DNA plant viruses and are among the most damaging pathogens causing epidemics in economically important crops worldwide. Wild/non-cultivated plants play a crucial epidemiological role, acting as begomovirus reservoirs and as 'mixing vessels' where recombination can occur. Previous work suggests a higher degree of genetic variability in begomovirus populations from non-cultivated hosts compared to cultivated hosts. To assess this supposed host effect on the genetic variability of begomovirus populations, cultivated (common bean, Phaseolus vulgaris, and lima bean, P. lunatus) and non-cultivated (Macroptilium lathyroides) legume hosts were intensively sampled from two regions across Brazil. A total of 212 full-length DNA-A genome segments were sequenced from samples collected between 2005 and 2012, and populations of the begomoviruses Bean golden mosaic virus (BGMV) and Macroptilium yellow spot virus (MaYSV) were obtained. We found, for each begomovirus species, similar genetic variation between populations infecting cultivated and non-cultivated hosts, indicating that the presumed genetic variability of the host did not a priori affect viral variability. The MaYSV population (N = 99) was more variable than the BGMV population (N = 147), which was explained by numerous recombination events in MaYSV. MaYSV and BGMV showed distinct distributions of genetic variation, with the BGMV population (but not MaYSV) being structured by both host and geography.
    Journal of General Virology 07/2014; 95(Pt_11). DOI:10.1099/vir.0.067009-0
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    • "The roles of mutation (Aranda et al., 1997; Malpica et al., 2002; Sanjuán et al., 2009; Tromas & Elena, 2010) and recombination (Aranda et al., 1997; Bonnet et al., 2005; Chen et al., 2002; Fernández-Cuartero et al., 1994; Froissart et al., 2005; Martín et al., 2009; van der Walt et al., 2009) in the evolution of plant RNA viruses have been studied extensively. Although it has been suggested widely that both high mutation and recombination rates are beneficial per se, they could also be byproducts of the parasitic lifestyle of viruses that favours fast replication over high fidelity (Belshaw et al., 2008; Elena & Sanjuán 2005) and of the modularity of viral RNA genomes (Martin et al., 2005; Simon-Loriere & Holmes, 2011). "
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    ABSTRACT: Phylogenomic evidence suggests that recombination is an important evolutionary force for potyviruses, one of the larger families of plant RNA viruses. However, mixed-genotype potyvirus infections are marked by low levels of cellular coinfection, precluding template switching and recombination events between virus genotypes during genomic RNA replication. To reconcile these conflicting observations, we have evaluated the in vivo recombination rate (r_g) of Tobacco etch potyvirus by coinfecting plants with pairs of genotypes marked with engineered restriction sites as neutral markers. The recombination rate was then estimated using two different approaches: (i) a classical approach that assumes recombination between marked genotypes can occur in the whole virus population, rendering an estimate of r_g = 7.762×1e8 events per nucleotide site per generation; (ii) an alternative method that assumes recombination between marked genotypes can occur only in coinfected cells, rendering a much higher estimate of r_g = 3.427×1e5 events per nucleotide site per generation. This last estimate is similar to the TEV mutation rate, suggesting that recombination should be at least as important as point mutation in creating variability. Finally, we compared our mutation and recombination rate estimates to those reported for animal RNA viruses. Our analysis suggests that high recombination rates may be an unavoidable consequence of selection for fast replication at the cost of low fidelity.
    Journal of General Virology 12/2013; 95(Pt_3). DOI:10.1099/vir.0.060822-0
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    • "Previous studies have indicated a high intra-and interspecific diversity of begomoviruses, which can facilitate adaptation to new climates and novel hosts (Monci et al., 2002). Recombination is the most intensively studied population genetic process in begomoviruses, and has been considered more significant than mutation by many researchers (Lefeuvre et al., 2007a, 2009; Martin et al., 2005, 2011; Monci et al., 2002; Padidam et al., 1999; Pita et al., 2001). It appears to heavily contribute to begomovirus genetic diversity, increasing the evolutionary potential and local adaptation of strains (Berrie et al., 2001; Graham et al., 2010; Harrison & Robinson, 1999; Monci et al., 2002; Padidam et al., 1999). "
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    ABSTRACT: Begomoviruses are single-stranded DNA plant viruses which cause serious epidemics in economically important crops worldwide. Non-cultivated plants also harbor many begomoviruses, and it is believed that these hosts may act as reservoirs and as mixing vessels where recombination may occur. Begomoviruses are notoriously recombination-prone, and also display nucleotide substitution rates equivalent to those of RNA viruses. In Brazil, several indigenous begomoviruses have been described infecting tomatoes following the introduction of a new biotype of the whitefly vector in the mid-1990's. More recently, a number of viruses from non-cultivated hosts have also been described. Previous work has suggested that viruses infecting non-cultivated hosts have a higher degree of genetic variability compared to crop-infecting viruses. We intensively sampled cultivated and non-cultivated plants in similarly sized geographic areas known to harbor either the weed-infecting Macroptilum yellow spot virus (MaYSV) or the crop-infecting Tomato severe rugose virus (ToSRV), and compared the molecular evolution and population genetics of these two distantly-related begomoviruses. The results reinforce the assertion that infection of non-cultivated plant species leads to higher levels of standing genetic variability, and indicate that recombination, not adaptive selection, explains the higher begomovirus variability in non-cultivated hosts.
    Journal of General Virology 11/2012; 94(Pt_2). DOI:10.1099/vir.0.047241-0
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