Constraints to Genetic Exchange Support Gene Coadaptation in a Tripartite RNA Virus

Abstract

Genetic exchange by recombination, or reassortment of genomic segments, has been shown to be an important process in RNA virus evolution, resulting often in important phenotypic changes affecting host range and virulence. However, data from numerous systems indicate that reassortant or recombinant genotypes could be selected against in virus populations and suggest that there is coadaptation among viral genes. Little is known about the factors affecting the frequency of reassortants and recombinants along the virus life cycle. We have explored this issue by estimating the frequency of reassortant and recombinant genotypes in experimental populations of Cucumber mosaic virus derived from mixed infections with four different pairs of isolates that differed in about 12% of their nucleotide sequence. Genetic composition of progeny populations were analyzed at various steps of the virus life cycle during host colonization: infection of leaf cells, cell-to-cell movement within the inoculated leaf, encapsidation of progeny genomes, and systemic movement to upper noninoculated leaves. Results indicated that reassortant frequencies do not correspond to random expectations and that selection operates against reassortant genotypes. The intensity of selection, estimated through the use of log-linear models, increased as host colonization progressed. No recombinant was detected in any progeny. Hence, results showed the existence of constraints to genetic exchange linked to various steps of the virus life cycle, so that genotypes with heterologous gene combinations were less fit and disappeared from the population. These results contribute to explain the low frequency of recombinants and reassortants in natural populations of many viruses, in spite of high rates of genetic exchange. More generally, the present work supports the hypothesis of coadaptation of gene complexes within the viral genomes.

Evolution and structure of Tomato spotted wilt virus populations: evidence of extensive reassortment and insights into emergence processes

“…3). showed that reassortment occurs at rather low rates in viruses of the family Bunyaviridae (Henderson et al, 1995;Nemirov et al, 1999) or of other families (Fraile et al, 1997;Lin et al, 2004;Roossinck, 2002;Bonnet et al, 2005;Miranda et al, 2000;Iturriza-Gó mara et al, 2001;Watanabe et al, 2001;McDonald et al, 2009), which could be due to strong selection acting against reassortants (Brown et al, 2002;Fraile et al, 1997;Escriu et al, 2007). Some viral taxa seem however to show more extensive reassortment (Silander et al, 2005;Lindstrom et al, 2004;Nelson et al, 2008;Khiabanian et al, 2009).…”

Diversity of Plant Virus Populations: A Valuable Tool for Epidemiological Studies

“…It has been shown that selection against heterologous gen combinations increases as host colonization progresses along the infection cycle of Cucumber mosaic virus [32], affecting the frequency of genetic exchange. This explains that recombinants and reassortants are often found at low frequencies [33,34], although the frequency of particular combinations may be dependent on agro-ecological factors [17,19], and support the hypothesis of co-adaptation of gene complexes within the viral genomes [32,35].…”

Questions and Concepts in Plant Virus Evolution: a Historical Perspective

“…This report also provides the only estimate of recombination rates, 2xl0 _5 -5xl0" 5 per base and replication cycle, i.e., on the order of mutation rates in RNA viruses (Froissart et al 2005). However, genetic structure of field RNA virus populations often indicates constraints to genetic exchange (Bonnet et al 2005), and experiments with both DNA and RNA vimses (Maize streak virus and CMV, respectively) have shown that heterologous gene combinations are selected against, supporting the coadaptation of gene complexes in viral genomes (Martin et al 2005;Escriu et al 2007). Thus, this is also evidence that epistatic interactions would constrain the plasticity of the small genomes of RNA vimses.…”